(Ardila, 2012) - On The Origins of Human Cognition

ON THE ORIGINS OF HUMAN COGNITION
Alfredo Ardila
Department of Communication Sciences and Disorders
Florida International University
Miami, Florida, USA
2012
CONTENT
1. Introduction
Statement of the Problem
References
15
2. Origins of Language
23
Introduction
23
There are only two fundamental aphasia syndromes
24
The selection disorder
25
The sequencing disorder
29
Other aphasia syndromes
30
Three stages in language development
36
Initial communication systems
37
The function of noises (grunts) in human communication
41
Second stage: Lexical/semantic
41
Third stage: Grammar
43
Brain representation of nouns and verbs
45
Memory systems for nouns and verbs
46
Using verbs and using grammar is a single ability
46
Understanding Brocas area
47
Origins of the lexical/semantic system
52
Origins of the grammatical system
54
Grammar at the origin of the executive functions
56
Conclusions
60
References
60
3. Origins of Spatial Abilities
81
Introduction
81
How we get oriented in the space?
83
Perceptual Constancy
83
Reference Systems
84
Cultural Differences in Visuoperceptual Abilities
85
Acquired spatial cognition disorders
86
Neuroimaging studies
89
Conclusions
92
References
93
4. Origins of Writing
100
Introduction
100
How did writing appear?
101
How many people can write?
106
Agraphia as a neuropsychological syndrome
107
Dysexecutive agraphia
Is any area in the brain specialized for writing?
108
108
Brain activation during writing
109
Writing in different systems
110
From agraphia to dystypia
113
Conclusions
117
References
118
5. Origins of Calculation Abilities
124
Introduction
124
Numerical concepts in animals
125
Development of calculation abilities in children
126
Numerical abilities in pre-school children
127
Development of numerical abilities at school
131
Calculation abilities in pre-historic man
132
Further developments of arithmetical abilities
142
The neuroscience of calculation abilities
147
Conclusion
150
References
151
6. Origins of Executive Functions
161
Introduction
161
What does executive functions mean?
162
Is there any fundamental core ability accounting for

executive functions?
167
Two proposed fundamental executive functions
169
Metacognitive executive functions as an internalization

of action
Is there anything special in the prefrontal cortex?
173
178
Executive functions in pre-historical man
181
Metacognitive executive functions as a cultural product
183
Tentative conclusions
184
References
186
7. How we recognize other people?
202
Introduction
202
Own-species members recognition
203
Gender recognition
208
Emotional expression and emotional recognition
210
Individuals' recognition
212
Conclusions
217
References
218
8. Culture and Cognitive Testing
230
Introduction
230
What is culture?
231
Why culture affects cognitive test performance?
233
Patterns of abilities
235
Cultural values
235
Familiarity
238
Language
239
Education
240
Culture minorities groups
246
Norms in different national and cultural groups
249
References
254
1. Introduction
Nothing in biology makes sense
except in the light of evolution
(Theodosius Dobzhansky, 1973)
Understanding the historical evolution of cognition represents a crucial question for our
interpretations of the human specie. This is a question that has been approached since
long ago by different classical authors, including Wundt (1863/1864), James (1890),
Vygotsky (1931), Luria (1974, 1976), Leontiev (1981), and many others, and still remains
an unsettled question. As a matter of fact, during the last decades, a myriad of books and
journal papers has been published (e.g., Ardila, 1993; Cummins & Allen, 1998; Heyes &
Huber, 2000; Parker & McKinney, 1999; Tomasello, 2001; Travis, 2007; Walsh, 2001;
Woods, 1996; Zimmer, 2005) approaching this question and attempting to shed light on
the origins of complex psychological processes, such as language, complex perception,
and executive functions. This is a question that in no way is easy to answer but is most
important for understanding the idiosyncrasies of our own specie. It is a question that can
be approached from different perspectives, including a neuropsychological one.
This book includes a collection of papers around the general question: How - from a
neuropsychological perspective -, did cognition emerge in human history?
Statement of the Problem
Anthropology has striven to understand how man's living conditions were 10,000, 100,000
or 1,000,000 years ago. The Stone Age (usually divided in the Old Stone Age or Paleolithic,
and New Stone Age or Neolithic) extended until some 3,000-6,000 years ago (Hours, 1982;
Toth & Schick, 2007). Agriculture appeared some 10,000 years ago; first cities some 6,000
years ago; first civilizations about 5,000 years ago; writing has only five or six thousand
years history; and arithmetical abilities, about 6,000 years (Childe, 1936; No author, 1993;
Sampson, 1985; Toth & Schick, 2007). But most important to bear in mind, when
considering that agriculture appeared some 10,000 years ago and writing has five or six
thousand years history, it does not mean that the whole human species began to live in
cities 10,000 years ago and to use written language five or six thousand years ago. It only
means that some few people began to live a sedentary life and to use written language.
The diffusion of the changes that occurred during the last 10,000 years has been a
particularly slow process. Nowadays, for instance, there are human groups that are still
nomads (regardless that the first cities were created some 10,000 years ago), and about
20% of the world population is illiterate (UNESCO, portal.unesco.org) (regardless that
writing was invented some five-six thousand years ago).
Contemporary man (Homo sapiens sapiens) has lived on the earth probably since
about 200,000 years ago (Wells, 2003; Wood, 1996; Zimmer, 2005). We can state, with
certain level of confidence, that during this time, his brain structural changes have been
minimal (Barkow, Cosmides & Tooby, 1992; Harris, 1983; Streidter, 2005). It is easy to
conclude that human brain adaptation was accomplished to survive more exactly in
Stone-Age life conditions (during about 99% of human technological history) than in those
existing nowadays. Only when departing from the analysis of these original living conditions
can we understand the specific characteristics and idiosyncrasies of his brain adaptation. It
would seem reasonable for any neuroscientist to raise the question: What type of
information processing abilities did the human brain become adapted for? Consequently,
which are man's basic or universal cognitive abilities?
The search for universals has guided an important proportion of the anthropological
and linguistic activity during the last decades. Anthropology and linguistics have departed
from three different approaches, attempting to reconstruct the way of life and the languages
spoken by the prehistorical man:
1. Archeological findings are used as elements to reconstruct prehistoric ways of life.
2. By comparing existing human groups, it is possible to find some common social,
behavioral, and linguistic characteristics. Those common characteristics that eventually are
disclosed most likely already existed in prehistorical times, and probably are the result of
man's specific biological adaptation. Several thousands of different cultures have been
described (Bernatzik, 1957; Harris, 1983), and contemporary man speaks close to 7,000
different languages (www.ethnologue.com). By comparing all these cultures and all these
languages, some universals can be discovered (Greenberg, 1978; Haviland, 2007;
Swadesh, 1971).
3. By taking existing cultures and/or living languages into consideration, similar in a
specific parameter to prehistorical cultures and/or languages, it is possible to propose how
prehistorical living forms and language characteristics could have been with regard to that
particular parameter.
These three approaches (to use archeological findings, to find common
characteristics when comparing different human groups, and to use an existing human
group, similar in a certain parameters to the prehistorical groups) are potentially useful,
and, as a matter of fact, have been used in neuropsychological research, although in a
restricted way.
1. We can attempt to reconstruct how some neuropsychological characteristics
may have been several thousand years ago, departing from some archeological
findings. For instance, we can study handedness in Neolithic man departing from
On the Origins of Human Cognition 10
pictorial rests (Spennemann, 1984).

2. We can search for commonality among existing groups. For example, we can
study aphasic language disturbances throughout different world languages, looking for
common characteristics and consequently, basic brain language organization (Menn &
Obler, 1990; Paradis, 2001). And finally,
3. We can study some neuropsychological variables in living human groups, similar
in a specific parameters to the prehistorical man. For instance, we can analyze illiteracy in
order to attempt to figure out how linguistic or praxic abilities were in pre-writing societies
(e.g., Ardila et al., 1989; Rosselli et al., 1990; Ardila et al., 2010; Lecours et al., 1987,
1988); or we can analyze constructional abilities among Stone Age-like Amazonian Indians
(Pontius, 1989).
Undoubtedly, neuropsychology has tremendously advanced in some specific areas;
for instance, in the assessment of the sequelae of brain pathology; or in the establishment
of clinical/anatomical correlations. Our fundamental and basic knowledge about the brain
organization of cognitive activity under normal and pathological conditions has significantly
advanced during the last decades thanks very specially to the use of contemporary
neuroimaging techniques (e.g., Cabeza & Nyberg, 2000; Brodmanns interactive atlas,
www.fmriconsulting.com/ brodmann/). Nevertheless, we do not have enough understanding
about what can be understood and what can be considered as "basic cognitive abilities".
Thus, for instance, classification of spatial cognition disturbances is still very confusing and
partially contradictory (e.g., De Renzi, 1982; Rizzolatti, Berti & Gallese, 2000; Robertson,
2003). We barely have dealt with individual differences in neuropsychological performance
(e.g., Hartlage & Telzrow, 1985). And our understanding of cultural differences is, to be
optimistic, very insufficient (Ardila, 1995; Fletcher-Janzen, Strickland & Reynolds, 2000;
Helm, 1992; Uzzell, Pontn & Ardila, 2007; Pedraza & Mungas, 2008).
Some significant interest toward cultural and historical issues, however, has recently
been observed in neuropsychology. However, this interest in obtaining a better
understanding of cultural and historical issues in the neuropsychology sphere is not new.
Some precursor attempts are found in literature. For instance, A.R. Luria is well-known in
neuropsychology for his contributions to the analysis of the brain organization of language;
or, his research on the prefrontal syndrome. However, his cultural approach to
neuropsychology is less recognized. Nonetheless, Luria departed from the analysis of
cultural issues (Luria, 1934, 1976; see Footnote 1) and only moved further toward
neuropsychology. Unfortunately, most of his cross-cultural research proposals in
neuropsychology (for example, the analysis of hemi-neglect syndrome in different cultural
groups; the cross-linguistic analysis of aphasias; the comparison of alexias in different
writing systems, etc.) never turned into concrete research programs. But his great interest
and emphasis on cultural and historical variables in neuropsychology was always reflected
in his writings.
During the last decades a significant number of papers devoted directly or indirectly
to the analysis of cultural variables on neuropsychological performance have been
recorded in literature. It could be mentioned: the bilingualism research (e.g., Albert & Obler,
1978; Dupont et al., 1992; Paradis, 1987, 2004; Vaid, 1986); the studies on illiteracy (e.g.,
Ardila et al., 1989, 2010; Lecours et al., 1987, 1988; Matute, 2000; Ostrosky et al., 1998;
Reis & Castro-Caldas,1998; Rosselli et al., 1990 ); the cross-linguistic analysis of aphasia
(e.g., Bates et al., 1987a, 1987b, 1988; Menn & Obler, 1990; Paradis, 2001); the research
about the influence of socioeducational factors in neuropsychological performance (e.g.,
Ardila et al., 2000; Ostrosky et al., 1985; Rosselli & Ardila, 1990); and the studies on
cultural variables on handedness (e.g., Ardila et al., 1989a; Bryden, 1987; Bryden et al.,
1993; Harris, 1990).
This collection of papers attempts to direct the attention of behavioral neurosciences,
toward some potentially relevant historical and cultural variables in neuropsychological
performance. The purpose of this book is, in consequence, multiple:
1 The book "Cognitive Development" was initially written in the 1930', but it was published in Russian only in
1974 with the name "About the Historical Development of Cognitive Processes". In 1976 it was translated to
English with the name "Cognitive Development: Its Cultural and Social Foundations"
1. To integrate some information regarding cross-cultural differences in

neuropsychological performance.
2. To review some evidence about the historical origins of cognitive activity.
3. To analyze how the inclusion of a historical and cultural perspective in behavioral
neurosciences can contribute to obtain a better understanding about the brain organization
of cognition. And, finally,
4. To propose some general guidelines for future research in the area.
Different problems are analyzed.
In the chapter Origins of Language it is emphasized that there are two
fundamental forms of aphasia which are linked to defects in the lexical/semantic and
grammatical systems of language (Wernicke-type aphasia and Broca-type aphasia,
respectively). Grammar correlates with the ability to represent actions (verbs) and depends
on what is known as Brocas area and its related brain circuits, but it is also related to the
ability to quickly carry out the sequencing of the articulatory movements required for
speaking (speech praxis). Language as a grammatical system seemingly appeared
relatively recently and seems to be exclusive to Homo sapiens.
The paper Origins of Spatial Abilities analyzes the development and
cross-cultural differences of spatial cognition. It is proposed that: (1) Spatial abilities are
found to be significantly associated with the complexity of geographical conditions and
survival demands; (2) spatial cognition has evolved in a parallel way with cultural evolution
and ecological demands; and (3) contemporary city-man may be using those spatial
abilities in some new, non-existing in pre-historical times, conceptual tasks (such as
mathematics, reading, writing, mechanics, music, etc.).
In the chapter Origins of Writing it is argued that there is no brain area

specialized for writing, but rather that writing relies on some basic abilities that existed long
before writing was invented. Pre-writing was initially a visuoconstructive and ideomotor
ability, and only later did it become the language-related ability of writing. It is also
emphasized that most of the neuropsychological syndromes, including agraphia, were
described during the late 19th and early 20th century, but living conditions have changed
dramatically during the last 100 years. Writing no longer means only using pencil and
paper, but also includes using computer word processing programs. Writing using paper
and pencil does not require the same cognitive, motor, and spatial tasks as those required
when using a computer keyboard. Although the conceptual knowledge of written language
can be the same, the motor activity and the spatial abilities that are used are rather
different. It can be anticipated that new neuropsychological syndromes resulting from these
new living conditions will be described in the future.
In the chapter Origins of Calculation Abilities it is pointed out that counting,
departing from finger sequencing, is observed in different ancient and contemporary
cultures, whereas number representation and arithmetic abilities are found only during the
last five-six thousand years. The paper analyzes the rationale of selecting a base of ten in
most numerical systems, and the clinical association between acalculia and finger agnosia.
Finger agnosia, right-left discrimination disturbances, semantic aphasia, and acalculia is
proposed to conform a single neuropsychological syndrome associated with left angular
gyrus damage. It is hypothesized that acalculia, finger agnosia, and disorders in right-left
discrimination (as in general, in the use of spatial concepts) result from the disruption of
common cognitive mechanisms.
In the paper Origins of Executive Functions it is proposed that the prefrontal
lobe participates in two closely related but different executive function abilities: (1)
metacognitive executive functions: problem solving, planning, concept formation, strategy
development and implementation, controlling attention, working memory, and the like; that
is, executive functions as they are usually understood in contemporary neuroscience; and
(2)
emotional/motivational
executive
functions:
coordinating
cognition
and
emotion/motivation (that is, fulfilling biological needs according to some existing conditions).
The first one depends on the dorsolateral prefrontal areas, whereas the second one is
associated with orbitofrontal and medial frontal areas. Current tests of executive functions
basically tap the first ability (metacognitive). Solving everyday problems (functional
application of executive functions), however, mostly requires the second ability
(emotional/motivational); therefore, these tests have limited ecological validity. Contrary to
the traditional points of view, recent evidence suggests that the human prefrontal lobe is
similar to other primates and hominids. Other primates and hominids may possess the
second (emotional executive functions) prefrontal ability, but not the first (metacognitive
executive functions) one. It is argued that metacognitive executive functions are
significantly dependent on culture and cultural instruments. They probably are the result of
the development and evolution of some conceptualization instruments; language (and
written language as an extension of oral language) may represent the most important one.
The second executive function ability (emotional/motivational) probably is the result of a
biological evolution shared by other primates.
The question of recognizing other individuals is further analyzed ("How we
recognize other people? "). It is emphasized that not only visual, but also auditory and
even olfactory information may be involved in people recognition. Visual information is
proposed to include not only the perception of faces, but also the perception of whole-body
and gait, clothes, emotional expressions, and individual marks. Departing from clinical
observation, a model for people recognition is presented. It is hypothesized that different
"subsystems" or "modules" may be involved in individuals' recognition: "living" versus
"nonliving", "own-species" versus "other-species", "familiar" versus "nonfamiliar", "males"
versus "females", and "individual identification" versus "emotional identification".
The chapter Culture and Cognitive Testing attempts to summarize the major
cultural variables affecting neuropsychological test performance. Initially, culture is defined
as the specific way of living of a human group, and further, the question why culture affects
cognitive test performance? is approached. Different cultural aspects potentially affecting

neuropsychological test performance are reviewed. The issues of familiarity, language and
education are also discussed. Cognitive testing of so-called minority groups is analyzed in
a special section. Finally, it is concluded that understanding the variables that can affect
cognitive test performance seems to be as important as obtaining a large number of norms
in different linguistic and cultural groups.
Finally, my sincere gratitude goes out to all the colleagues and friends who
encouraged me to write this book. I want to thank Florida International University for the
opportunity to write this book during my sabbatical year. My gratitude to Natasha
Aiguesvives for her editorial support. I sincerely hope that this collection of papers will
further the interest in the analysis of historical and cultural variables in cognition, and will
contribute to the development and strengthening of cross-cultural neuropsychology. No
doubt, cross-cultural neuropsychology represents a critical new direction of research, and
will challenge neuropsychologists during the coming years.
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2. Origins of Language
Introduction
For many years, the origin of human language has been a controversial topic and different
explanatory proposals have been presented (e.g., Atkinson, 2011; Bickerton, 2009;
Christiansen & Kirby, 2003; Nowak & Komarova, 2001). At a certain point in history, the
debate became so complex and hot, that in 1866 the Linguistic Society of Paris banned
discussion of the origin of language, arguing that it is to be an unanswerable problem.
Contemporary research on linguistics, archeology, comparative psychology and
genetics has significantly advanced in understanding the origins of human language (e.g.,
Bickerton, 1990; Corballis, 2002; Enard et al., 2002; Mallory, 1989; Nowak & Krakauer,
1999; Ruhlen, 1994; Scott-Phillips, 2010; Swadesh, 1967; Tallerman, 2005). Different
disciplines have contributed from their own perspective to make the human communication
system more comprehensible.
The purpose of this chapter is not to further review and discuss the historical origins
of language, but to relate what is known (or supposed) on the origins of language, with
contemporary neurology and neuropsychology data, particularly in the area of aphasia.
Aphasia knowledge can potentially make a significant contribution to the understanding
about the origin and evolution of human language.
Initially, some basic neuropsychological data about language impairments in the
case of brain pathology will be presented. It will be emphasized that there are two basic
linguistic operations (selecting and sequencing; i.e., language as a paradigm and language
as a syntagm) (Jacobson & Halle, 1956; Jacobson, 1971). There are also two basic types
of aphasia syndromes named in different ways (e.g., motor/sensory; anterior/ posterior;
nonfluent/ fluent; Broca-type/ Wernicke-type; encoding /decoding disorder; expressive/
receptive disorder, etc.), each one related with the disturbance of one of these two basic
language elements (lexical/semantic and grammatical) (for a review, see Ardila, 2010).
Hence, in considering language evolution these two different dimensions of language have
to be recognized. Each one may have emerged at a different historical moment. Analyzing
this basic distinction and including it in an interpretation about language evolution can
potentially further language evolution understanding.
There are only two fundamental aphasia syndromes

Since the XIX it is well known that there are two major aphasic syndromes (see Table 2.1),
named in different ways, but roughly corresponding to Wernicke-type aphasia and Brocatype aphasia (e.g., Albert et al., 1981; Bastian, 1898; Benson & Ardila, 1996; Freud,
1891/1973; Goldstein, 1948; Head, 1926; Hcaen, 1972; Kertesz, 1979; Lichtheim, 1885;
Luria, 1976; Pick, 1931; Schuell et al., 1964; Taylor-Sarno, 1998; Wilson, 1926). These two
major aphasic syndromes have been related to the two basic linguistic operations: selecting
(language as paradigm) and sequencing (language as syntagm) (Jacobson & Halle, 1956;
Jacobson, 1971; Luria, 1972/1983). Jacobson (1964) proposed that aphasia tends to
involve one of two types of linguistic deficiency. A patient may lose the ability to use
language in two rather different ways: the language impairment can be situated on the
paradigmatic axis (selection or similarity disorder; Wernicke-type aphasia) or the
syntagmatic axis (contiguity or sequencing disorder; Broca-type aphasia).
It is important to emphasize that when Dejerine (1914) first proposed the concept of
language zone or language area in the brain, he referred indeed to three areas: Brocas
area, Wernickes areas, and the angular gyrus (involved in written language) (Figure 2.1.).
Thence, he recognized two brain areas related with spoken language and one cortical area
participating in written language. But the point is that for Dejerine it was clear that there are
two different spoken language areas in the brain: Brocas area and Wernickes area, and
consequently, there are two fundamental types of acquired language disorders.
________________________________________________
expressive
receptive
motor
sensorial
anterior
posterior
no fluent
fluent
paradigmatic impairment
syntagmatic impairment
coding impairment
decoding impairment
Wernicke-type
Broca-type
________________________________________________
Table 2.1. Different names used to refer to the two basic aphasic syndromes.
The selection disorder

The selection (similarity) disorder restricts the patients ability to select words from the
paradigmatic axis. These patients (Wernicke-type aphasia) cannot find words that exist as
parts of the system (vocabulary). These aphasics have severely limited access to this
language repertoire system. Specific nouns tend to be inaccessible and more general ones
(cat becomes animal) take their place. These patients cannot select among alternative
names (dog, cat, fox, etc). These patients may instead fill out their discourse with
circumlocutions (the clock is referred as to know the time"). Words no longer have a
generic (paradigmatic) meaning for these patients, so verbal expressions tend to be
strongly contextualized, and speech becomes empty. A dog can be referred as animal,
it barks, fox, etc.
Figure 2.1. The language zone in the brain (Dejerine, 1914.)
Luria (1972/1983) emphasized that the selection disorder can be observed at

different levels of the language, corresponding to different aphasia subtypes: phoneme
selection (aphasia acoustic agnosic), word selection (aphasia acoustic amnesic), and
meaning selection (amnesic aphasia). By the same token, the contiguity disorder can be
observed at different levels: sequencing words (kinetic motor aphasia Broca aphasia) or
sequencing sentences (dynamic aphasia transcortical motor aphasia). Noteworthy,
different subtypes of Wernicke aphasia are frequently distinguished (e.g., Ardila, 2006).
Lurias acoustic agnosic, acoustic amnesic, and amnesic aphasia are indeed subtypes of
the language impairment syndrome referred to as a whole as Wernicke aphasia.
In Wernicke aphasia, the lexical repertoire tends to decrease and language
understanding difficulties are evident. Wernicke aphasia patients do not fully discriminate
the acoustic information contained in speech. Lexical (words) and semantic (meanings)
association become deficient. Patients have problems in recalling the words (memory of the
words) and also in associating the words with specific meanings. Consequently, it is evident
that at least three different deficits underlie Wernicke-type aphasia: (1) phoneme
discrimination defects, (2) verbal memory defects, and finally (3) lexical/semantic
association deficits. Figure 2.2 presents the model proposed by Ardila (1993) to account for
the language recognition defects observed in cases of Wernicke-type of aphasia.
In Wernicke-type aphasia obviously the language defect is situated at the level of the
meaningful words (nouns). Phoneme and word selection are deficient, but language syntax
(contiguity: sequencing elements) is well preserved and even overused (paragrammatism
in Wernicke aphasia).
Nouns seem to depend on an organized pattern of brain activity. Contemporary
clinical and neuroimaging studies have corroborated that different semantic categories are
differentially impaired in cases of brain pathology. For instance, in anomia it has been
traditionally recognized that naming body-parts, external objects and colors depend (and
are altered) upon the activity of different brain areas (Hcaen & Albert, 1978). It has also
been found that finer distinctions can be made with regard to naming defects, which can be
limited to a rather specific semantic category (e.g., peoples names, living things, tools,
geographical names, etc) (e.g., Harris & Kay, 1995; Goodglass et al., 1986; Lyons et al.,
2002; Warrington & Shallice, 1984) and even as specific as medical terms (Crosson et al.,
1997). A brain mapping of the memory organization of different semantic categories could
be supposed.
Long -term memory

for features
ear
B
Primary auditory
analysis
Frequency intensity
recognition
Short -term memory

for features
Long -term memory

for phonemes
Features recognition
Phoneme recognition
Categorical
perception
language recognition
level I
I
Short -term memory
for phonemes
J
Verbal -acoustic long
memory
term
K
Verbal -acoustic
recognition (lexical)
Categorical
perception
level II
L
Verbal acoustic short
memory
-term
M
Associations
(visual, tactile, etc)
N
Semantic
Recognition
Categorical perception
level III
Figure 2.2. Diagram model for language recognition proposed by Ardila (1993).Three
levels of language recognition potentially impaired in Wernicke-type aphasia can be
distinguished: phonemic (categorical perception level I),
lexical (categorical
perception level II), and semantic (categorical perception level III). Three different
sub-syndromes can be found: phonemic discrimination defects (acoustic-agnosic or
Wernicke aphasia type I), verbal-acoustic memory defects (acoustic-amnesic or
Wernicke aphasia type II), and semantic association defects (amnesic, nominal or
Extrasylvian sensory aphasia).
The sequencing disorder

Broca-type of aphasia represents the clinical syndrome characterized by impairments in the
sequencing process (syntagmatic axis defect). It is usually recognized that Broca aphasia
has two different distinguishing characteristics: (a) a motor component (lack of fluency,
disintegration of the speech kinetic melodies, verbal-articulatory defects, etc., that is usually
referred as apraxia of speech); and (b) agrammatism (e.g., Benson & Ardila, 1996; Luria,
1976; Goodglass, 1993; Kertesz, 1985). If both defects are simultaneously observed (i.e.,
they are very highly correlated), it simply means they both are just two different
manifestations of a single underlying defect. It is not easy to understand which one could
be the single factor responsible for these two clinical manifestations; but it may be kind of
an "inability to sequence expressive elements" (Figure 2.3).
Broca aphasia
Apraxia of speech
Agrammatism
ability to sequence expressive elements ?
Factor
Figure 2.3. A single factor (probably the ability to sequence expressive elements)
can underlie the two disturbances observed in Broca aphasia (Ardila & Bernal, 2007).
A single common factor underlying both defects should be assumed. Broca's area,
most likely, is not specialized in producing language, but in certain neural activity that can
support not only skilled movements required for speech, but also morphosyntax. It is
interesting to note that deaf-mute subjects (who, in consequence have never produced
verbal articulatory movements) present a virtually total impossibility to learn, understand,
and use language grammar (Poizner et., 1987). Probably, the lack of verbal articulatory
normal development is necessarily associated with a lack of normal grammatical
development.
Other aphasia syndromes

Some aphasic syndromes can eventually be considered as variants of the Broca and
Wernicke aphasia. For instance, amnesic or anomic or nominal aphasia (usually due to
damage in the vicinity of Brodmanns area 37) (Hcaen & Albert, 1978; Head, 1926; Luria,
1976) can be interpreted as a subtype of Wernicke aphasia in which the semantic
associations of the words are significantly impaired (see Figure 2.4). Luria himself during a
long time was unsure if amnesic aphasia should be regarded an independent aphasia
syndrome; or rather, it should be considered simply as a subtype of the sensory aphasia
(in addition to the acoustic-agnostic and acoustic-amnesic subtypes). During a long time,
Luria referred to six different types of aphasia (e.g., Luria, 1966, 1970) and suggested a
seventh one. Only in his later writings (e.g., Luria, 1976) he overtly referred to seven
different types of aphasia.
Figure 2.4. Amnesic or nominal or extrasylvian sensory aphasia can be interpreted

as a paradigmatic disturbance situated at the level of semantic recognition.
Some other aphasic syndromes can be interpreted as language disturbances due to

a more general underlying disorder. For instance, extrasylvian (transcortical) motor aphasia
associated with left convexital prefrontal damage could be interpreted as an executive
function defect specifically affecting the language use. The ability to actively and
appropriately using the language (pragmatics) appears impaired while the phonology,
lexicon, semantics, and grammar are preserved. Simply speaking, the question is: should
the ability to correctly use language be regarded as a linguistic ability (i.e., cognitive ability)
as executive function ability?(i.e., metacognitive ability). It does not seem difficult to argue
that the ability to correctly use the language can be interpreted as an executive function
and as a metacognitive ability rather than a purely linguistic ability. Some rationales to
support this interpretation are: (1) It could be argued that in extrasylvian (transcortical)
motor aphasia there is a defect in verbal initiative rather than in language knowledge
(Kleist, 1934). (2) Some authors (Luria, 1976, 1980) have emphasized that this type of
aphasia shares the general characteristics of the prefrontal (i.e., dysexecutive) syndrome
but specifically with regard to the verbal processes. That means it is the prefrontal
(dysexecutive) syndrome affecting the verbal processes. (3) Further, the language defect in
extrasylvian (transcortical) motor aphasia does not affect the language understanding, and
the fundamental linguistic processes are preserved (Berthier, 1999). And finally, (4) it could
be argued that the prefrontal cortex does not participate in basic cognition but in
metacognition (e.g., Ardila & Surloff, 2010). Extrasylvian (transcortical) motor aphasia could
indeed be referred as dysexecutive aphasia. Some authors have interpreted extrasylvian
motor aphasia in a similar way (e.g., Luria, 1976, 1980). Alexander (2006) suggested that
transcortical motor aphasia could be more accurately defined as an executive function
disorder than as an aphasia. He proposed that the progression of clinical disorders from
aphasia to discourse impairments can be interpreted as a sequence of procedural
impairments from basic morpho-syntax to elaborated grammar to narrative language,
correlated with a progression of the focus of the damage from posterior frontal to polar
and/or lateral frontal to medial frontal.
Conduction aphasia, on the other hand, usually has been interpreted as a
disconnection syndrome (e.g., Damasio & Damasio, 1980; Geschwind, 1965; Wernicke,
1874) usually due to an impairment in the arcuate fasciculus and sporadically in an indirect
pathway passing through inferior parietal cortex (Catani et al., 2005) (Figure 2.5).
Alternatively, conduction aphasia has also been interpreted as a segmentary ideomotor
apraxia (e.g., Ardila & Rosselli, 1990; Brown, 1972, 1975; Luria, 1976, 1980).
Usually it is recognized that conduction aphasia has three fundamental and five
secondary characteristics; so-called secondary characteristics are frequently but not
necessarily found in conduction aphasia (Benson et al., 1973; Benson & Ardila, 1996). The
three basic characteristics are: (1) fluent conversational language; (2) almost normal
comprehension; (3) significant impairments in repetition. Secondary characteristics include,
(1) defects in naming; (2) reading defects; (3) variable writing difficulties (apraxic agraphia);
(4) ideomotor apraxia; (5) neurological abnormalities.
Figure 2.5. Conduction aphasia frequently is interpreted as a disconnection between

the Wernickes and Brocas areas, due to an interruption of the arcuate fasciculus.
This description of conduction aphasia clearly recognizes that spontaneous language

production and language understanding are significantly preserved. In consequence, some
mechanism required for the correct language repetition is abnormal, but the knowledge of
the language itself (phonology, lexicon, semantics, and grammar) is not impaired. Should
conduction aphasia be interpreted as a primary aphasic syndrome? Obviously, if some
animals can repeat, that means that language repetition cannot be considered as a primary
linguistic ability.
Bernal and Ardila (2009) pointed out that as a matter of fact the arcuate fasciculus
does not connect Wernickes area with Brocas area (BA44), but more exactly with the
premotor area (BA6); hence, there is not a direct connection between Wernickes and
Brocas area, as illustrated in Figure 2.6.
Figure 2.6. Recent findings suggest that there is not a direct connection between
Wernickes and Brocas areas, but there is a relay station located in the precentral
gyrus, represented here by the circle labeled BA6, an area with premotor functions
(Taken from Bernal & Ardila, 2009).
Conduction aphasia is not really a primary form of aphasia but rather a secondary
(or peripheral) defect in language affecting a specific language ability (i.e., the ability to
repeat). The language itself is not impaired, but rather the ability to reproduce the auditory
information that is heard aloud is impaired. Of course, this is a most important ability used
not only to develop but also to correctly use language (moreover, the correct visualperceptual recognition of the written information is a most important ability required not only
for learning to read but also for correctly accessing the written information).
Jakobson (1964) suggested a similar distinction when proposed that in aphasia,
language could be either disintegrated or just limited (disintegration vs. limitation in
aphasia). Obviously, in conduction aphasia language is limited, not really disintegrated.
Tabla 2.2. presents the aphasia classification proposed by Ardila (2010). A major
distinction in aphasia can be established between primary language disturbances (central
aphasias), and secondary language disturbances resulting from peripheral impairments
(secondary or peripheral aphasias). Sometimes language is not impaired, but the patient
cannot use it appropriately because of executive control impairments (dysexecutive
aphasia).
____________________________________________________________________________
Type
Impairment
____________________________________________________________________________
Primary (central) aphasias
Language system impaired
Wernicke-type aphasia (fluent aphasia)
Phonological level
Lexical level
Semantic level
Broca-type aphasia (non-fluent aphasia)
Sequencing expressive elements at syntactic and

phonetic level
___________________________________________________________________________
Secondary (peripheral) aphasias
Mechanisms of production impaired
Conduction aphasia
Disconnection (or segmentary ideomotora verbal

apraxia)
SMA aphasia
To initiate and maintain voluntary speech

production
___________________________________________________________________________
Dysexecutive aphasia
Language executive control impaired
Extra-Sylvian (transcortical) motor aphasia Executive control of language

___________________________________________________________________________
Tabla 2.2. Only two primary aphasic syndromes are recognized: Wernicke-type
aphasia (fluent aphasia) and Broca-type aphasia (non-fluent aphasia). Two
secondary aphasia syndromes are included (conduction aphasia and aphasia of the
supplementary motor area); finally, a dysexecutive (extrasylvian or transcortical
motor) aphasia is also included (Ardila, 2010).
Three stages in language development

The question When language began? could be rephrased as the question How language
began? Different steps in language development can be proposed, at least:
(1) Initial communication systems using sounds and other types of information such
as gestures, etc, similar to the communication systems observed in other animals, including
nonhuman primates.
(2) Primitive language systems using combined sounds (words) but without a
grammar (language as lexical/semantic system). This type of language could be similar to
the holophrasic period in language development, observed in children around the age 1 to
1.5 years of age (Hoff, 2003).
(3) Communication systems using grammar (language as grammatical system).
During childs language development, it is observed that the use of grammar is found after
the holophrasic period. It simply means that it is a more advanced and complex stage. By
the end of the second year, children begin to combine words into simple sentences. Initially,
sentences represent a telegraphic speech (around 24-30 months of age), including twoword utterances in which connecting elements are omitted (e.g., other dog", child eat)
(Hoff, 2003). It means, language initially emerges as a system of words (language as a
paradigm: lexical/semantic system), and only later as a system of relations among the
words (language as a syntagm: grammatical system).
Initial communication systems

It is easy to assume that at the beginning of the human language, communication systems
were similar to the communication systems found in nonhuman primates. It is known that
chimpanzees and other nonhuman primates in natural environments can use some
communication strategies.
Chimpanzees employ a variety of gestures and facial expressions to communicate
and keep in touch with each other. They possess a simple repertoire of noises and
postures (body language) that can be used in different contexts with specific
communication purposes. Observations have been collected in different environments,

including natural environments and captive groups in human-controlled environments
(McCrone, 1991). Chimpanzees make use of simple gestures, make facial expressions and
produce a limited amount of vocalizations. Compared to humans, chimps only produce
about twelve different vocalizations. In captive conditions and under human training,
chimpanzees can learn some artificial languages and close to about 200 words (symbols).
Different attempts have been made to teach non human primates to use a more
complex communication system. Initially, Hayes and Hayes (1952) trained the chimp Vicki.
She became able to produce only four different sounds in six years! (mom," "pa," "cup,"
and "up"). Other chimps and gorillas have also participated in communication training
programs: Nim and Koko used signs; Sara used plastic chips; Lana, Sherman, and Austion
manipulated combinations of buttons to communicate (Gardner & Garner, 1979; Limber
1982; Patterson & Linden, 1981).
Regardless of the relatively large amount of meaningful elements that chimpanzees
can learn, they fail in developing sequencing of elements (grammar). Kanzi learned to use
around 200 symbols on a portable electronic symbol board. While chimpanzees can learn
to order their symbols to get what they want, it is not clear that they have mastered syntax
(Mitani, 1995; Savage-Rumbaugh & Lewin, 1994). The reason is that when they initiate
communication, they often abandon the order of phrases they have learned and the order
is rather random.
There have been occasional reports of chimpanzees signing new combinations of
words in response to new situations. Washoe, for example, once was in a boat on a pond
when she encountered her first duck. She signed 'water bird' (Terrace, 1979). This could be
a new compound noun or it could be two separate responses to the water and a bird. But
between two nouns, there is not a grammatical relationship and hence no grammar is
involved in 'water bird'.
In conclusion, there is not convincing evidence that chimpanzees and other
nonhuman primates can learn language syntax (language as syntagm) even after intensive
and controlled training.
The question becomes how can this type of simple communication system found in
subhuman primates in natural conditions (i.e., to use some few vocalizations, gestures and
facial expressions) be further developed into contemporary human language? Certain
mechanisms potentially could be used; e.g., words can be created departing from
onomatomepias, emotional expressions, etc. Indeed, a diversity of mechanisms has been
proposed throughout history to account how human words emerged. It means that different
strategies could potentially be useful to create words. This is an ability that is not found in
nonhuman primates. Using these strategies certainly requires a brain notoriously more
advanced than the chimpanzees brain.
During the 19th century different hypotheses were presented in an attempt to explain
the origin of language from the lexical point of view. Jespersen (1922) referred to such
hypotheses using some unusual names as a way of deriding the hypotheses as simplistic
speculation. However, these names became popular and they have been used even in
contemporary literature. Some hypotheses are (Yule, 1996):
1. Language began as imitations of natural sounds. It means that words are created
departing from onomatopoeias (bow-wow hypothesis).
2. Language began with interjections, emotive cries, and emotional expressions
(Pooh-pooh hypothesis).
3. Gestures are at the origin of language, and body movement preceded language.
Oral language represents the use of oral gestures that began in imitation of hand gestures
that were already in use for communication (ta-ta hypothesis). Recently, Corballis (2002)
has argued that gestures represent the most important element in creating human
language.
4. Language arose in rhythmic chants and vocalisms uttered by people engaged in
communal labor. Language began as rhythmic chants, perhaps ultimately from the grunts
of heavy work or related with assistance or cooperation accompanied by appropriate
gestures (Yo-he-ho hypothesis).
5. Language began with the easiest syllables attached to the most significant objects
(mama hypothesis).
6. It has been pointed out that there is a certain correspondence between sounds
and meanings. Small, sharp, high things tend to have words with high front vowels in many
languages, while big, round, low things tend to have round back vowels. This is often
referred to as phonetic symbolism (ding-dong hypothesis).
7. It has been also suggested that language comes out of play, laughter, cooing,
courtship, emotional mutterings and the like (The sing-song hypothesis)
8. Considering that there is a need for interpersonal contact, language may have
began as sounds to signal both identity (here I am!) and belonging (Im with you!) (contact
theory) (hey you hypothesis).
All these hypotheses may be partially true, and all these factors may have
contributed to the creation of new words. As a matter of fact, these hypotheses attempt to
explain how the initial communication systems (observed in nonhuman primates) evolved to
the second stage in language evolution: the development of a lexical system, which
potentially can be transmitted to offspring. But they do not account for the development of
grammar. These mechanisms for creating new words continue being useful in the
contemporary world. For instance, onomatopeias continue representing a mechanism in the
creation of new words (e.g., the ping-pong game). The phonetic symbolism is particularly
useful in the creation of adjectives (qualities of the objects).
The function of noises (grunts) in human communication

No mention about the function of noises (grunts) in human everyday communication is
readily available. As noted above, noises represent a basic communication strategy in
chimpanzees, and noises have continued playing a communication function throughout
human history. It is evident that people in everyday life use a diversity of noises to say
yes, no, to express different emotions, to communicate with animals (e.g., come here,
go away), etc. These noises are close to interjections, and sometimes become real
interjections (e.g., ooph!). Even though there is not a dictionary of noises, the author of
this paper has been able to identify over 30 different noises commonly used in
contemporary Spanish language. Some of these noises seem understandable by speakers
of other languages, but others seem idiosyncratic of Spanish-speaking people.
Second stage: Lexical/semantic

Bickerton (1990) developed the idea that a protolanguage must have preceded the fullfledged syntax of todays discourse. Echoes of this protolanguage can be seen, he argued,
(1) in pidgin languages, (2) in the first words of infants, (3) in the symbols used by trained
chimpanzees, and (4) in the syntax free utterances of children who do not learn to speak at
the normal age. Bickerton (2009) considers that such a protolanguage existed already in
the earliest Homo (about 2.3 to 2.4 million years), and was developed due to the pressure
of the behavioral adaptations faced by Homo habilis (2.3 to 1.4 million years ago).
What made up these original words? Again, the analogy with the childs initial
vocabulary can be taken. (1) They were articulatory easiest to produce, most likely using
those phonemes regarded as universal (e.g., /p/, /a/). (2) They contained a simple syllable
structure (consonant-vowel) that may have been repeated (e.g., papapa). In this regard,
they were similar to the infantile words. (3) They were mostly nouns (real objects) even
though they obviously did not have a grammatical category.
To move from grunts, onomatopoeias, and emotional expression to words requires
the progressive development of a series of oppositions. According to Jacobson (1968) the
most basic one is the opposition between vowels and consonants. The second most
important one is between oral and nasal articulations. But the production of these
oppositions requires some anatomical adaptations.
Human articulatory ability has been related to the specific position and configuration
of the larynx. The human larynx descends during infancy and the early juvenile periods,
and this greatly contributes to the morphological foundations of speech development. This
developmental phenomenon is frequently believed to be unique to humans. However,
Nishimura (2003; Nishimura et al., 2005) demonstrated that chimpanzees larynges also
descend during infancy, as in human infants. This descent was completed primarily through
the rapid descent of the laryngeal skeleton relative to the hyoid, but it was not accompanied
by the descent of the hyoid itself. The descent is possibly associated with developmental
changes of the swallowing mechanism. Moreover, it contributes physically to an increased
independence between the processes of phonation and articulation for vocalization. Thus,
the descent of the larynx and the morphological foundations for speech production must
have evolved in part during hominoid evolution and not in a single shift during human
evolution.
Several authors have attempted to find universal language characteristics, and even
to reconstruct extinct languages (e.g., Greenberg, 1978; Hagge, 1982 ; Van den Berghe
1979) such as the Indo-European (Anderson, 1973; Lehmann, 1974; Martinet, 1975;
Shevoroshkin, 1990), whose last speaker passed away over 10,000 years ago.
Furthermore, examples of which ones could have been the initial words in human language
have been proposed. Swadesh (1971) refers to the communality existing in some words
across the world. Although we cannot be sure which were the initial words used by
humans, there are clues about the initial meaning sounds and approximately, how the initial
words may have been formed.
Third stage: Grammar

What was the crucial leap for the development of grammar? (i.e., syntagmatic dimension of
the language). Obviously grammar was initially simple, and sentences contained only two
words. How to link two words to create new higher level unit (syntagm)? Further, how to
mark the relationship between the two words? The mechanism has to be the simplest one,
and it is not unlikely that it may be similar to the mechanism observed in children during
language development.
Suppose that we have two lexical units:
-animal - fruit
Different relations between these two words can exist; but the relationship requires
an action (verb); it means that there is an interaction between both elements: animal eats
fruit; animal has fruit, animal receives fruit; animal likes fruit, etc.
In consequence, before creating a syntagmatic relationship between the words,
different word categories have to be separated (e.g., objects and actions). According to the
Swadesh word list (1952, 1967), the following categories are found across different
languages, and may represent the initial word categories: (1) Grammatical words (e.g.,
I/me), (2) Quantifiers (e.g., All), (3) Adjectives (e.g., Big), (4) Human distinctions (e.g.,
person), (5) Animals (e.g., fish), (6) High frequency elements (e.g., tree), (7) Body parts
(e.g., hair), (8) Actions (e.g., drink), (9) Natural phenomena (e.g., sun), and (10) Colors
(e.g., red).
For creating a phrase, only two types of elements are really required: nouns
(nominal phrase) and verbs (verbal phrase). When putting together two words
corresponding to two different classes (e.g., animal sleep), there is already a syntagm and
grammar that has appeared. In childhood language it is observed that words corresponding
to two different classes are combined such as, big dog, food good, dad gone. They
contain a grammar because the words belong to two different classes. In the first two
examples, there is an existence verb (to be) that is omitted (as currently observed in some
contemporary languages, such as Russian). Mom dad is not a phrase, but mom big is a
primitive sentence.
Brown (1973) found that the majority of the utterances at the beginning of the childs
grammar could be described by a small set of functional relationships between words:
1.
'agent + action' baby kiss
2.
'action + object' pull car
3.
'agent + object' daddy ball
4.
'action + location' sit chair
5.
'object + location' cup table
6.
'possessor + possession' mommy sock
7.
'object + attribute' car red
8.
'demonstrative + object' there car
So, the crucial point in emerging grammar is not the extension of the vocabulary.
What really is crucial is to have words corresponding to different classes that can be
combined to form a higher level unit (syntagm). One of the words has to be a noun; the
other usually is a verb.
Hence, the problem becomes how do verbs appear? Creating nouns does not seem
so complicated using the hypothesis mentioned above (e.g., nouns can be created
departing from onomatopoeias, etc). Verbs, on the other hand, can be created departing
from the nouns, but with the meaning of an action (e.g., baby kiss). Action usually means
moving, doing, executing, not simply perceiving and associating with some visual (or
auditory or tactile) information. Kiss can be associated with some sensory information,
and obviously the temporal, parietal and occipital brain areas have to participate (kiss as a
noun). Kiss can also be associated with an action, and obviously the frontal areas have to
be involved in this second type of association (kiss as a verb).
Brain representation of nouns and verbs

It has been observed that choosing verbs and nouns clearly depends on different brain
area activity, and naming objects and actions are disrupted in cases of different type of
brain pathology. While speaking or thinking in nouns increased activity is observed in the
temporal lobe, while speaking or thinking verbs activates the Broca frontal area (Raichle,
1994). By the same token, impairments in finding nouns are associated with temporal lobe
pathology, whereas impairments in finding verbs is associated with left frontal damage and
Broca aphasia (Ardila & Rosselli, 1994; Damasio & Tranel, 1993)
Naming actions activates the left frontal operculum roughly corresponding to the
Brocas area (Damasio et al., 2001). The neural correlates of naming concrete entities such
as tools (with nouns) and naming actions (with verbs) are partially distinct: the former are
linked to the left inferotemporal region, whereas the latter are linked to the left frontal
opercular and left posterior middle temporal regions (Tranel et al., 2005). Furthermore, the
pattern of brain activation when processing verbs seems similar across languages, at least
in Spanish/English bilinguals (Willms et al., 2011). However, understanding action verbs
does not rely on early modality-specific visual or motor circuits. Instead, word
comprehension relies on a network of amodal brain regions in the left frontal, temporal, and
parietal cortices that represent conceptual and grammatical properties of words (Bedny &
Caramazza, 2011). Supposedly, interactions between word meanings and sensory-motor
experiences occur in higher-order polymodal brain regions.
Memory systems for nouns and verbs

Two major memory systems are frequently distinguished in contemporary memory
literature: declarative memory (divided into semantic and episodic or experiential) and
procedural memory (Tulving et al., 2004). It has been suggested that the lexical/semantic
and grammar aspects of the language are subserved by different neuroanatomic brain
circuitries and depend upon these two different memory systems (Fabbro, 1999, 2001;
Paradis, 2004; Ullman, 2001; 2004). Whereas lexical/semantic aspects of the language
depend on a declarative semantic memory (knowledge about the meaning of the words),
grammar depends on a procedural memory.
The lexical/semantic aspect of the language is explicitly learned and represents a
type of knowledge we are aware of (declarative memory). It depends on retro-rolandic
cortical structures and the hippocampus. Grammar (language sequences, contiguity) is
acquired incidentally. Procedural memory for grammar supposes implicit language
knowledge. Procedural grammatical learning is related to the execution of sequences of
elements (skilled articulatory acts and grammar) used for speaking but also for syntax.
Procedural memory is related with frontal/subcortical circuitries (Tulving et al., 2004).
Using verbs and using grammar is a single ability

Brocas area damage results in a defect in grammar and also in an inability to find verbs. In
consequence, brain representation of actions and brain representation of grammar is
coincidental. Using verbs and using grammar depends upon the very same type of brain
activity and both are simultaneously disrupted in cases of Broca aphasia. It can be
conjectured that verbs and grammar appeared almost simultaneously in human language;
or rather, they are the two sides of the same medal. Furthermore, grammar is associated
with oral praxis skills (i.e., agrammatism and apraxia of speech appear simultaneously in
Broca aphasia), and hence, all three have to appear simultaneously in the evolution of
human language: using verbs, using grammar, and rapidly sequencing movements with the
articulatory organs.
However, there is a departing condition for using verbs, namely, the ability to
internally represent actions. That is, to interiorize the actions. The obvious question is: can
Broca aphasia patients internally represent actions? Although specific research on this
question is not readily available, the answer seems to be no. Some observations point to a
deficit in internally representing actions in Broca aphasia. For example, Ardila and
Rossellis (1994) patient had to make the concrete action to retrieve the corresponding
verb. Thence, the internal representation of actions and understanding/using verbs seems
to be closely related abilities.
Understanding Brocas area

In the last decade there has been a significant interest in re-analyzing the function of
Brocas area (e.g., Grodzinsky & Amunts, 2006; Hagoort, 2005; Thompson-Schill, 2005).
So-called Brocas area includes the pars opercularis (Brodmanns area- BA- 44) and
probably the pars triangularis (BA45) of the inferior frontal gyrus (Foundas, 1998) (see
Figure 2.7). BA45 probably is more cognitive than BA44, which seems to be more motor,
more phonetic. From the traditional point of view, Brocas area corresponds to BA44, but
several contemporary authors also include BA45. In the traditional aphasia literature it was
assumed that damage in the Brocas area was responsible for the clinical manifestations
observed in Brocas aphasia. Only with the introduction of the CT scan did it become
evident that the damage restricted to the Brocas area was not enough to produce the
classical Brocas aphasia; extension to the insula, lower motor cortex, and subjacent
subcortical and periventricular white matter is also required (Alexander et al., 1990).
Brocas area aphasia (minor Brocas aphasia) is characterized by mildly non-fluent
speech, relatively short sentences and mild agrammatism; phonetic deviations and a few
phonological paraphasias can be observed (Mohr, et al., 1978); some foreign accent can
also be noticed (Ardila et., 1988). Interestingly, electrical stimulation of Broca's area
enhances implicit learning of an artificial grammar (de Vries et al., 2010) and can also
modulate naming skills (Fecteau et al., 2011) and is active during speech perception
(Vaden et al., 2011).
Figure 2.7. Map illustrating the Brodmanns areas (BA).
Simultaneously including both BA44 and BA45 in Brocas area is problematic. BA 44

is a premotor dysgranular area, whereas BA45 has a granular layer IV and belongs to the
heteromodal prefrontal lobe (granular cortex) (Mesulam, 2002). So, from a
cytoarchitectonic point of view, BA 44 and BA 45 are quite different. BA 44 is a premotor
area whereas BA 45 corresponds to the prefrontal cortex. From the aphasia perspective,
some authors have referred to different clinical manifestations associated with damage in
BA 44 (Broca-type aphasia) and BA 45 (transcortical motor/dynamic aphasia) (e.g., Luria,
1976). Brocas area is, more than likely, involved in different language and language related
functions (Fink et al., 2006). Some authors have pointed out that indeed Brocas area is a
collective term that can be fractionated in different sub-areas (Lindenberg et al., 2007).
Hagoort (2005, 2006) refers to the Brocas complex, including BA44 (premotor), and also
BA45 and BA47 (prefrontal cortex). He argues that Brocas complex is not a languagespecific area, and it becomes active during some nonlanguage activities, such as mental
imagery of grasping movements (Decety et al., 2004). Functional defined sub-regions could
be distinguished in the Brocas complex: BA47 and BA45 are involved in semantic
processing, BA44, BA45, and BA46 participate in syntactic processing, and BA44 is
involved in phonological processing (Heim et al., 2008; Sahin et al., 2009). Hagoort (2005)
proposes that the common denominator of the Brocas complex is its role in selection and
unification operations by which individual pieces of lexical information are bound together
into representational structures spanning multiword utterances (p. 166). Its core function
is, consequently, binding the elements of the language. Thompson-Schill (2005) analyzed
the different deficits observed in cases of damage in the Brocas area: articulation, syntax,
selection, and verbal working memory, suggesting that there may be more than a single
function of Brocas area.
Thompson-Schill (2005) analyzed the different deficits observed in cases of damage
in the Brocas area: articulation, syntax, selection, and verbal working memory, suggesting
that there may be more than a single function of Brocas area. The author proposes a
framework for describing the deficits observed in different patients. The proposed
framework suggests that Brocas area may be involved in selecting information among
competing sources. Fadiga et al. (2006) speculates that the original role played by Brocas
area relates to generating/extracting action meanings; that is, organizing/ interpreting the
sequence of individual meaningless movements. Ardila and Bernal (2007) conjectured that
the central role of Brocas area was related to sequencing motor/expressive elements.
Novick et al. (2005) consider that the role of Brocas area is related with a general cognitive
control mechanism for the syntactic processing of sentences.
Grodzinsky (2000, 2006) has presented an extensive analysis of the role of Brocas
area. He proposed that most syntax is not located in Brocas area and its vicinity
(operculum, insula, and subjacent white matter). This brain area does have a role in
syntactic processing, but a highly specific one: it is the neural home to receptive
mechanisms involved in the computation of the relation between transformationally moved
phrasal constituents and their extraction sites (syntactic movement). He further assumes
that Brocas area is also involved in the construction of higher parts of the syntactic tree in
speech production. Interestingly, blood flow in Brocas area increases when participants
process complex syntax (Caplan et al., 2000). Santi and Grodzinsky (2007) also recognize
its role in working memory related with a specific syntactic role in processing fillergaps
dependency relations. Syntax is indeed neurologically segregated, and its components are
housed in several distinct cerebral locations, far beyond the traditional ones (Brocas and
Wernickes regions). A new brain map for syntax would also include portions of the right
cerebral hemisphere (Grodzinsky & Friederici, 2006).
Haverkort (2005) emphasizes that a clear distinction should be established between
linguistic knowledge and linguistic use. Patients with Brocas aphasia have a limitation in
the use of grammar, but their grammatical knowledge is available. Brocas aphasia patients
present a simplified syntax and phrases are usually short. They select simpler syntactic
structures that are less complex because they impose a lesser burden on working memory.
In consequence, one major factor in Brocas aphasia relates to impairment in verbal
working memory.
In summary, regardless that expressive language disturbances have been
associated for over a century with damage in the left inferior frontal gyrus (later known as
Brocas area), currently there is incomplete agreement about its limits and its specific
functions in language. Different proposals have been presented to explain language

disturbances in so-called Brocas aphasia, as summarized in Table 2.3.
_______________________________________________________________________________
Function
Reference
_______________________________________________________________________________
Binding the elements of the language
Haverkort, 2005
Selecting information among competing sources
Thompson-Schill, 2005
Generating/extracting action meanings
Fadiga et al., 2006
Sequencing motor/expressive elements
Ardila & Bernal, 2007
Cognitive control mechanism for syntactic processing sentences
Novick et al., 2005
Construction higher parts syntactic tree in speech production
Grodzinsky, 2000, 2006
Verbal working memory
Haverkort, 2005
_______________________________________________________________________________
Table 2.3. Different proposals about the role of Brocas area.
As emphasized above, language activity depends on two discrete brain areas (socalled Wernickes and Brocas areas). Damage in these two brain regions results in
disturbances in language as a paradigm (similarity: selection; lexical/semantic system) and
syntagm (contiguity: combination; grammatical system).
At what moment in human history did the first and the second aspect of language
emerge? There is not a simple answer, but obviously language as a lexical/semantic
system appeared before language as a grammatical system.
Pre-human communication systems continue playing a role in contemporary human
communication. Onomatopoeias continue representing a source for the creation of new
words. Noises and gestures are actively used nowadays in everyday communication.
Origins of the lexical/semantic system

Paleoneurology (study and analysis of fossil endocasts) can also significantly contribute to
the understanding of the origins of the language. How did the brain areas participating in
human lexical/semantic knowledge (i.e., temporal lobes) evolve? In monkeys, the temporal
lobes are involved in recognizing the sounds and calls of their own species (Rauschecker
et al., 1995; Taglialatela et al., 2009; Wang et al., 1995; Wollberg & Newman, 1972), and
obviously the temporal lobe was a crucial area in developing a complex lexical/semantic
system.
Gannon et al (1998) observed that the anatomic pattern and left hemisphere size
predominance of the planum temporale, a language area of the human brain, are also
present in chimpanzees. They found that the left planum temporale was significantly larger
in 94 percent of chimpanzee brains examined. Hence, the crucial lexical/semantic
difference between humans and chimpanzees cannot be related to the planum temporale.
By the same token, it has been observed that anatomical temporal lobe asymmetries
favoring the left hemisphere are found in several Old and New world monkey species
(Heilbroner & Halloway, 1988). Development of a human lexical/semantic communication
system cannot be related with the temporal lobe asymmetry, because this asymmetry was
observed long before the beginning of the human language.
Hopkins and Nir (2010) examined whether chimpanzees show asymmetries in the
planum temporale for grey matter volume and surface area in a sample of 103
chimpanzees from magnetic resonance images. The results indicated that, overall, the
chimpanzees showed population-level leftward asymmetries for both surface area and grey
matter volumes. Furthermore, chimpanzees that prefer to gesture with their right-hand had
significantly greater leftward grey matter asymmetries compared to ambiguously- and lefthanded apes. Development of a human lexical/semantic communication system in
consequence cannot be related to the temporal lobe asymmetry, because this asymmetry
is observed long before the beginning of the human language. This asymmetry seems to be
related with a left temporal lobe specialization for intra-specific communication system.
Spocter et al. (2010) affirm that leftward asymmetry of Wernicke's area originated prior to
the appearance of modern human language and before our divergence from the last
common ancestor.
Nonetheless, differences can be related with the temporal lobe volume. Rilling et al.
(2002) analyzed the volume of the temporal lobe in different primates. Whole brain, T1weighted MRI scans were collected from 44 living anthropoid primates spanning 11
species. The surface areas of both the entire temporal lobe and the superior temporal
gyrus were also measured, as was temporal cortical gyrification. Allometric regressions of
temporal lobe structures on brain volume consistently showed apes and monkeys to scale
along different trajectories, with the monkeys typically lying at a higher elevation than the
apes. Within the temporal lobe, overall volume, surface area, and white matter volume
were significantly larger in humans than predicted by the ape regression lines. The largest
departure from allometry in humans was for the temporal lobe white matter volume which,
in addition to being significantly larger than predicted for brain size, was also significantly
larger than predicted for temporal lobe volume. Among the nonhuman primate sample,
Cebus have small temporal lobes for their brain size, and Macaca and Papio have large
superior temporal gyri for their brain size. The observed departures from allometry might
reflect neurobiological adaptations supporting species-specific communication in both
humans and old world monkeys. The authors concluded that the entire human temporal
lobe and some of its component structures are significantly larger than predicted for a
primate brain of human size. The most dramatic allometric departure is in the volume of the
human temporal lobe white matter, which, in addition to being large relative to brain size, is
also large relative to temporal lobe size. These allometric departures in humans could
reflect a reorganization of the temporal lobes driven by expansion of the language cortex
and its associated connections. In primates it is interesting to note that the superior
temporal gyrus contains neurons tuned to species specific calls, and the magnitude of
different species residuals might relate to the repertoire of vocal communicative signals as
reflections of the complexity of their respective social environments.
It has been calculated that this enlargement of the temporal lobe occurred some
200-300 thousand years ago (Kochetkova, 1973). Consequently, it can be conjectured that
hominids existing before the contemporary Cro-Magnon Homo sapiens could have
developed a certain complex lexical/semantic communication system. For instance, it could
be speculated that Nearthental man could have had a language relatively complex as a
lexical/semantic system.
Brain organization of the lexicon seems to be related with the type of association
between words and perceptions. When the word is associated with own-body information,
brain representation of the lexicon seems associated with a parietal extension (e.g., bodyparts names); when the word has just a visual association, an occipital extension is found
(Roux et al., 2006)
Origins of the grammatical system

Departing from the above observations, it can be speculated that grammar, speech praxis
movements, and using verbs appeared roughly simultaneously in human history. In other
words, they are strongly interrelated and depend upon a common neural activity.
Recently, a milestone observation was made that significantly enlightened our
understanding about the origin of language in general and grammar in particular. In
England a family, usually referred as the KE family, was found. In over three generations of
this family, about half the family members had presented a significant disturbance in
language development. Speech was largely unintelligible, and they were taught sign
language as a supplement to speech as children. Affected members presented severe
disturbances in articulation and other linguistic skills along with broader intellectual and
physical problems. From the genetic point of view the disorder was associated with a
mutation in a single autosomal-dominant gene, FOXP2, located in the chromosome 7

(Vargha-Khadem et al., 1995). The disorder was not restricted to speech and also included
the following characteristics: defects in processing words according to grammatical rules;
understanding of more complex sentence structure such as sentences with embedded
relative clauses; inability to form intelligible speech; defects in the ability to move the mouth
and face not associated with speaking (relative immobility of the lower face and mouth,
particularly the upper lip); and significantly reduced IQ in the affected compared with the
unaffected in both the verbal and the non-verbal domain.
Further, affected family members presented a pronounced developmental verbal
dyspraxia. The authors refer to the core deficit as one involving sequential articulation and
orofacial praxis (Takahashi & Liu, 2009; Vernes et al., 2006; Vargha-Khadem et al., 1998).
PET studies revealed functional abnormalities in both cortical and subcortical motor-related
areas of the frontal lobe, while quantitative analyses of MRIs revealed structural
abnormalities in several of these same areas, particularly the caudate nucleus, which was
found to be abnormally small bilaterally. An abnormal gene (SPCH1) in the chromosomal
band 7q31 was localized. The genetic mutation or deletion in this region was proposed to
result in marked disruption of speech and expressive language, including grammar (Fisher
et al., 1998).
Enard et al. (2002) analyzed the evolution of the chromosome FOXP2. They noted
the extremely conservative nature of FOXP2. The mouse FOXP2 differs in just one amino
acid from chimpanzee, gorilla and rhesus monkey. However, human FOXP2 differs from
gorilla, chimp and rhesus macaque in two further amino acids (and thus differs from mouse
in three amino acids out of 715). So, in 75 million years since the divergence of mouse and
chimpanzee lineages only one change occurred in FOXP2, whilst in the six million years
since the divergence of man and chimpanzee lineages two changes have occurred in the
human lineage. The authors estimated that the last two mutations occurred between
10,000 and 100,000 years ago and speculated that the mutations have been critical for the
development of contemporary human speech.
This genetic approach to the origins of language seems particularly important in
understanding the appearance and evolution of language in humans (Scharff & Petri, 2011;
Tanabe et al., 2011). It has been pointed out that FOXP2 could have contributed to the
evolution of human speech and language by adapting cortico-basal ganglia circuits (Enard,
2011). Although Foxp2 is expressed in many brain regions and has multiple roles during
mammalian development, the evolutionary changes that occurred in the protein in human
ancestors specifically affect brain regions that are connected via cortico-basal ganglia
circuits (Reimers-Kipping et al., 2011).
Grammar at the origin of the executive functions

So-called executive functions represent one of the most intensively studied neuroscience
questions during the last decade (e.g., Garcia-Molina et al., 2010; Koechlin et al., 2003;
Miller & Cohen, 2001; Stuss & Knight, 2002; Stuss & Levine, 2002). Disagreement persists,
however, around the potential unitary factor in executive functions (Mikaye et al., 2000;
Stuss & Alexander, 2007). Ardila (2008) emphasized that action representation (i.e.,
internally representing movements or actions) may constitute at least one basic executive
function factor. It could be speculated that action representation and also time
perception (potentially derived from action representation) may depend upon one single
core ability (sequencing?).
Two departing observations are important to support the involvement of prefrontal
cortex in motor representation:
(a) Anatomical observation. Prefrontal cortex represents an extension and further
evolution of the frontal motor areas (Miller &. Cummings, 2007; Risberg, 2006). It may be
conjectured that the prefrontal lobe should participate in complex and elaborated motor
(executive) activities.
(b) Clinical observation. A diversity of motor control disturbances are observed in

prefrontal pathology, such as perseveration, utilization behavior, paratonia, primitive
reflexes, etc. (e.g., Ardila & Rosselli, 2007; Victor & Ropper, 2001).
Throughout recent history several authors have argued that thought, reasoning, and
other forms of complex cognition (metacognition) depend on an internalization of actions.
Vygotsky (1929, 1934/1962, 1934/1978) for instance, proposed that thought (and in
general, complex cognitive processes) is associated with some inner speech. Vygotsky
represents the most classical author suggesting this interpretation for complex cognition.
More recently, Lieberman (2002a,b) suggested that language in particular and cognition in
general arise from complex sequences of motor activities.
The central point in Vygotskys (1934/1962) idea is that higher forms of cognition
(cognitive executive functions) depend on certain mediation (language, writing or any
other); the instruments used for mediating these complex cognitive processes are culturally
developed. According to Vygotsky (1934/1962) the invention (or discovery) of these
instruments will result in a new type of evolution (cultural evolution), not requiring any
further biological changes. Thinking is interpreted as a covert motor activity (inner
speech). Vocalization becomes unnecessary because the child thinks the words instead
of pronouncing them. Inner speech is for oneself, while external social speech is for others.
In brief, Vygotsky (1934/1978) argued that complex psychological processes
(metacognitive executive functions) derives from language internalization. Thinking relies in
the development of an instrument (language or any other) that represents a cultural
product.
Lieberman (2002a,b) refers specifically to the origins of language. He postulates that
neural circuits linking activity in anatomically segregated populations of neurons in
subcortical structures and the neocortex throughout the human brain regulate complex
behaviors such as walking, talking, and comprehending the meaning of sentences. The
neural substrate that regulates motor control (basal ganglia, cerebellum, and frontal cortex)
in the common ancestor of apes and humans most likely was modified to enhance cognitive
and linguistic ability. The cerebellum and prefrontal cortex are also involved in learning
motor acts (e.g., Matsumura et al., 2004; Hernandez-Mueller et al., 2005). Lieberman
(2002a,b) proposes that the frontal regions of the cortex are implicated in virtually all
cognitive acts and the acquisition of cognitive criteria; posterior cortical regions are clearly
active elements of the brains dictionary. Real-word knowledge appears to reflect stored
conceptual knowledge in regions of the brain traditionally associated with visual perception
and motor control. Some aspects of human linguistic ability, such as the basic conceptual
structure of words and simple syntax, are phylogenetically primitive and most likely were
present in the earliest hominids. Lieberman (2002a,b) further suggests that speech
production, complex syntax, and a large vocabulary developed in the course of hominid
evolution, and Homo erectus most likely talked, had large vocabularies, and commanded
fairly complex syntax.
These two authors (Vygotsky and Lieberman), although using rather different
approaches, have both postulated that the development of language and complex cognition
are related with some motor programs, sequencing, internalizing actions, and the like.
Many other authors have presented a similar point of view (e.g., (Hommel et al., 2001;
Jeannerod, 1997; Luria, 1969; Morsella et al., 2009; Prinz, 1999). Some contemporary
research seems to support this interpretation; for instance, Clerget et al. (2009) using
transcranial magnetic stimulation to interfere transiently with the function of left BA44 in
healthy individuals found that a virtual lesion of left BA44 impairs individual performance
only for biological actions, and more specifically for object-oriented syntactic actions. The
authors concluded that these finding provide evidence that Broca's area plays a crucial role
in encoding complex human movements, a process which may be crucial for understanding
and/or programming actions.
The recent discovery of mirror neurons (Di Pellegrino et al., 1992; Rizzolatti & Arbib,
1998; Rizzolatti et al., 1996) could significantly contribute to the understanding of the brain
organization for verbs. A mirror neuron is a neuron which fires both when an animal
performs an action and also when the animal observes the same action performed by
another animal. Mirror neurons were initially observed in monkeys (Di Pellegrino et al.,
1992), but in humans, brain activity consistent with mirror neurons has been found in the
premotor cortex and the inferior parietal cortex (Rizzolatti et al., 1996; Rizzolatti &
Craighero, 2004). These neurons (mirror neurons) appear to represent a system that
matches observed events to similar, internally generated actions.
Transcranial magnetic stimulation and positron emission tomography (PET)
experiments suggest that a mirror system for gesture recognition indeed exists in humans
and includes Brocas area (Rizzolatti & Arbib, 1998). The discovery of mirror neurons in
Brocas area might have important consequences for understanding brain language
organization and language evolution (Arbib, 2006; Craighero et al., 2007). An obvious
implication of mirror neurons is that they can participate in the internal representation of
actions, and the internal representation of actions may represent the origin of grammar.
Neuroimaging data have shown that interactions involving Brocas area and other cortical
areas are weakest when listening to spoken language accompanied by meaningful speechassociated gestures (hence, reducing semantic ambiguity), and strongest when spoken
language is accompanied by self-grooming hand movements or by no hand movements at
all, suggesting that Brocas area may be involved in action recognition (Skipper et al.,
2007). PET studies have associated the neural correlates of inner speech with activity of
Brocas area (McGuire et al., 1996). De Zubicaray et al. (2010) emphasize the importance
of Brocas area to covert verbalization. Clerget et al. (2009) using transcranial magnetic
stimulation to interfere transiently with the function of left BA44 in healthy individuals found
that a virtual lesion of left BA44 impairs individual performance only for biological actions,
and more specifically for object-oriented syntactic actions. The authors concluded that
these finding provide evidence that Broca's area plays a crucial role in encoding complex
human movements, a process which may be crucial for understanding and/or programming
actions. Conversely, left BA 44 plays a role in motor sequence learning (Clerget et al.,
2011).
In brief, there is some converging evidence that something like action
representation may constitute the departing point for both grammar and executive
functions.
Conclusions
Aphasia can contribute to the understanding of human language evolution. According to
contemporary aphasia knowledge, in cases of brain pathology, language can be disturbed
in two rather different ways: as a lexical/semantic system (Wernicke-type aphasia) and as a
grammatical system (Broca-type aphasia). Both language systems not only depend upon
different brain areas (temporal and frontal), but also upon different types of learning
(declarative and procedural) supported by different neuroanatomical circuitries.
Observations with childrens language development and experiments with nonhuman
primates demonstrate that language initially appears as a lexical/semantic system.
Grammar is correlated with the ability to represent and use actions. This is an ability that
depends on the so-called Brocas area and related brain circuits. But this ability also
depends, is correlated, and likely appeared simultaneously in human history with the ability
to rapidly sequence articulatory movements (speech praxis).
While the lexical/semantic language system may have appeared during human
evolution long before the contemporary man, the grammatical language system probably
represents a relatively recent acquisition. Language grammar may be the departing ability
for the development of the metacognitive executive functions and is probably based in the
ability to internally represent actions.
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3. Origins of Spatial Abilities
Introduction
Contemporary city life, in which direct orientation in space has been replaced by the logical
application of mathematical coordinates, represents not just a recent cultural acquisition,
but also, it is found only in some contemporary human groups. For a very long time,
education consisted of learning how to get oriented in the space, how to recognize the
relevant signals to follow prey, and how to move in the surrounding environment. This, of
course, is still valid for contemporary people living in the Amazonian jungle, for Eskimos, for
desert inhabitants, and many other world inhabitants. For thousands (and even millions) of
years, mans survival depended on the correct interpretation of spatial signals, memory of
places, calculation of distances, and so forth, and his brain must have become adapted
precisely to handle this type of spatial information (Ardila & Ostrosky, 1984).
Paleolithic (prehistorical era characterized by the development of the first stone
tools) extended since about 2,500,000 years (first hominids using stone tools) until some
10,000 years ago (Childe, 1936; Hours, 1982; Toth & Schick, 2007). About this time,
agriculture appeared, and man began to domesticate and raise some animals. This
produced a tremendous change in his way of life (the Neolithic Revolution). Paleolithic
represents in consequence about 99% of human technology history. That means, for about
99% of history, humans were nomads, and the correct spatial orientation represented the
most crucial ability for surviving.
It could be conjectured that biological adaptation was accomplished to survive under
those conditions existing during the Paleolithic time. Recent mans evolution corresponds in
a significant extent to a cultural type of evolution, not necessarily requiring further overt
biological changes. Agriculture replaced fruit collection; domestication of animals replaced
hunting; written language extended oral language; arithmetic extended finger counting; and
the use of maps and logical spatial coordinates replaced the direct orientation in space
(Vygotsky, 1962).
There is evidence that Australopitecus africanus (probably the direct ancestor of
Homo) lived on open savannas. Although his ancestors lived in forests, he moved to live in
open fields (Lee & DeVore, 1968; Wilson, 1975). He strongly depended on animal food,
especially small preys (tortoises, lizards, snakes, rabbits) and fruit collecting. Homo sapiens
appeared in Europe about 50,000 years ago (middle Paleolithic), and it is supposed that he
hunted, usually small but also big prey, used rudimentary stone tools (knives, axes), and
lived in caverns or rudimentary shelters built with tree branches. He was a nomad and he
had to be moving from one place to another all the time while looking for prey, fruits, and
shelter. He created some hunting weapons like the arrow and the spear, and used fire
(Washburn, 1978; Hours, 1982; Boyd & Silk, 2003).
It could be supposed that spatial abilities were even more crucial for survival in
prehistorical than in contemporary man. Survival in current urban living conditions
somehow requires different cognitive abilities. We go around in our cities using
logical-mathematical coordinates, reading a printed-on-a-paper map, without taking into
consideration the sun position in the sky, or avoiding potential predators. Adaptation to
contemporary world conditions requires more verbally-based abilities. If the question "What
moon-phase is today?" (instead of "What date is today?") was included in a mental state
examination, it is very likely the majority of city people would probably fail. By the same
token, city people usually ignore the exact sunrise and sunset points (they usually respond
"East and West"), but sunrise and sunset points change a little every day, and it could have
been an important piece of information for prehistorical man's survival, as it is for
contemporary man to know that "Today is May 6th, 2011." Furthermore, our current
educational system strongly emphasizes verbal, logical, and mathematical abilities, not
spatial orientation abilities. Of course, those are currently the most useful abilities to live in
our contemporary world. Generally speaking, city people have limited opportunities to
develop and use spatial orientation abilities.
How we get oriented in the space?

Cross-cultural differences in spatial orientation strategies under normal and pathological
conditions could be illustrative to understand how pre-historical man could have used
spatial information. Furthermore, it could shed some light about the potential spatial abilities
that contemporary man possesses. Brain organization of spatial abilities under pathological
conditions has been extensively studied in contemporary schooled Western (particularly
European and North American) people. To my best knowledge, however, no clinical
observations about disturbances in spatial abilities associated with brain pathology in other
(non-Western) culture have ever been reported.
Characteristics of spatial abilities in different cultures can be illustrative. Perceptual
constancy (stability of perception despite changes in the actual characteristics of the
stimuli) represents the most fundamental ability in the interpretation of the surrounding
spatial environment (Ardila, 1980; Walsh & Kulikowski, 1998).
Perceptual Constancy
In general, cross-cultural comparisons have demonstrated that perceptual constancy (size
and shape constancy) is more accurate in low-schooled and non-Western societys people
than in literate and westernized subjects (Pick & Pick, 1978). Beveridge (1940)
demonstrated a greater constancy of shape and size among West African adults than
among British adults. Myambo (1972) observed almost perfect shape constancy in
uneducated Malawi adults, whereas the educated Africans and Europeans did not perform
so accurately. Perceptual constancy may be expected to have been high (and crucial for
survival) not only in pre-historical man, but also to be high in people currently requiring a
complex interpretation of the surrounding spatial environment.
Reference Systems
People living in different environments develop different systems of spatial reference
(rivers, mountains, sun position, streets, buildings, etc). Geographic features affect the
terms of local reference systems, and differences in reference systems may, in turn, be
related to differences in perception of spatial orientation (Pick & Pick, 1978). The analysis
of different reference systems can be illustrative.
Gladwin (1970) analyzed the system used by Puluwat sailors to navigate among
clusters of islands in the Western Pacific. He disclosed that many different features of the
sea and sky comprise the information of which the system is based. Knowledge of the
habits of local sea birds provides cues for one's location. The sailors learn to defect the
coral reefs formation changes, which of course, differ depending on the conditions of the
weather, sea and sky. Ability to detect change in the "feel" of the boat moving through the
waves on a particular course is a skill used to maintain a course. There is a complex
reference system based on the position and patterns of stars in the night sky, and the rules
for navigating between specific islands are described in terms of the star patterns and
islands. Parallax information is also explicitly included in the system as descriptions of the
way in which the islands "move" as the boat passes on one or the other side of them (Pick
& Pick, 1978).
Amazonian Indians simultaneously use a variety of different types of information to
move around in the jungle. They use small rivers, orientation and color of trees, soil
characteristics, sun position, animal routes, olfactory cues, and many other signals to move
in the jungle. Vegetation is mildly different when closer to rivers, moss grows different in
trees according to the sun direction, and directions of river-flows are different. Additionally,
when moving in the jungle, they permanently break small bush branches, to recognize later
they have already crossed (and approximately how long time ago) that particular point. All
these environmental signals are simultaneously interpreted for getting oriented and moving
around the jungle.
Evidently, members of different cultures dwelling in different spatial environments
operate in terms of complex spatial reference systems, depending on their particular
demands and geographic environments. Demands and geographic environment were quite
different in Paleolithic times than they currently are for contemporary city-man. Evidently,
spatial orientation and reference systems used by pre-historical man were closer to
Puluwat sailors' or Amazonian Indians' reference systems than to our contemporary
orientation system in cities.
Cultural Differences in Visuoperceptual Abilities

Cross-cultural differences in perceptual abilities have been extensively studied and can be
particularly illustrative to understand perceptual skills in pre-historical man (Brislin, 1983;
Laboratory of Comparative Human Cognition, 1983; Segall, 1986). Hudson (1960, 1962)
studied depth perception using pictures that contained figures of an elephant, an antelope,
and a man with a spear; the basic question referred to what the man was doing with the
spear. There were four pictures differing with respect to the cues available for the
interpretation of the picture. This set of pictures was used with different groups of people
from Africa and Europe. It was observed that European children around 7-8 years have a
great difficulty perceiving the picture as three-dimensional. However, around 12 years,
virtually all children perceived the picture as three-dimensional. Not so with Bantu or
Guinean children. Nonliterated Bantu and European laborers responded to the picture as
flat,
not
three-dimensional.
They
cannot
interpret
represented-on-a-paper
three-dimensional figures; this also holds true in general for illiterate people (Ardila et al.,
1989). However, as mentioned above, illiterate African people do better than Western
literate subjects in perceptual constancy tasks with real objects. But they do worse when
the external space is represented on a paper.
Berry (1971, 1979) proposes that hunting people with specific ecological demands
usually present good visual discrimination and excellent spatial skills. For instance, the
embedded figures tests are better performed by cultural groups for whom hunting is
important for survival. Berry emphasizes that ecological demands and cultural practices are
significantly related to the development of perceptual and cognitive skills. A good example
of a specific culture-dependent cognitive skill was that reported by Gay and Cole (1967);
when Kpelle farmers are contrasted with American working class, the former were
considerably more accurate in estimating the amount of rice on several bowls of different
sizes containing different amounts of rice. By the same token, any cattle farmer is able to
accurately calculate the weight of a cow; or any dactylographist can easily and quickly
distinguish two different fingerprints; or any neurologist can distinguish a Parkinsonian
patient at one glance. Demands and training history are strongly associated with
visuoperceptual abilities.
Spatial abilities differ among cultures and depend on the specific ecological
demands. In neuropsychology, the perceptual ability disturbances of a very limited
subsample of the human species -contemporary Western, and most often, urban and
literate brain-damaged individuals have been relatively well analyzed. Nevertheless, our
understanding of the brain organization of spatial abilities, and their disturbances in cases
of brain pathology, are necessarily not only partial but, doubtless, biased. Norms for
perceptual performance in a sufficiently broad array of neuropsychological tests and an
extended analysis of perceptual disturbances in different cultural and ecological contexts
are required.
Acquired spatial cognition disorders

Visuospatial impairments resulting from brain damage have been extensively analyzed in
neuropsychology (e.g., De Renzi, 1982, 1985; Hcaen, 1962; Morrow & Ratcliff, 1988;
Newcombe & Ratcliff, 1989; Rosselli, 1986; Stiles, Stiles-Davis, Kritchevsky & Bellugi,
1988; Beis
et al., 2003; Hodgson & Kennard, 2003; Vallar, 2007). Different brain
syndromes have been distinguished.

Spatial agnosia represents an impairment in the perception and use of
spatial-dependent information resulting from brain pathology. It refers to an acquired
inability to recognize and integrate spatial information, regardless that there is not a primary
sensory defect capable to explain it (Ardila & Rosselli, 1992). Spatial agnosia includes
impairments in the recognition of line orientation, defects in depth perception, impairments
in handling spatial information, and deficits in spatial memory (De Renzi, 1983; Hcaen &
Albert, 1978).
Different types of spatial agnosia have been distinguished. Holmes (1918) separates
different categories of spatial agnosia: defects in objects localization, topographic amnesia,
inability to count objects, inability to perceive movement, loss of stereoscopic vision, and
deficits in eye movements. Critchley (1968) includes the following groups: (1) disorders in
spatial perception with regard to the three-dimensional perception, (2) disorders in spatial
concepts, and (3) disorders in spatial manipulation, which includes disorders in
topographical memory, defects in orientation, and unilateral spatial agnosia. Hcaen (1962)
proposed to separate: (1) disorders in spatial perception, (2) defects in spatial manipulation,
including, the loss of topographical concepts, and unilateral spatial agnosia, (3) loss of
topographical memory, and (4) Balint's syndrome. De Renzi (1982, 1985) presents some
modifications to Hcaen's classification. Balint's syndrome is included within visual
exploration disorders, and instead of disorders in manipulation of spatial information,
introduces the group of disorders in spatial thought. Table 3.1 presents the classification of
spatial agnosias proposed by Ardila and Rosselli (2007).
It is interesting to emphasize that all these disorders appear (mainly or exclusively)
in cases of right hemisphere pathology. That means the right hemisphere seems to be
specialized in spatial cognition. Language and ideomotor praxic abilities developed in left
brain areas that in the right brain are involved in spatial cognition (LeDoux, 1984).
Supposedly, similar spatial cognition disturbances are to be found in a similar way in
every individual, regardless of the cultural background and the ecological demands.
However, not only commonality but also differences would be expected to be found. If the
degree (not the direction) of brain lateralization of language depends on literacy, and in
general, on the verbal training history (Lecours et al., 1987, 1988; Matute, 1988), it would
seem reasonable to suppose that the degree of lateralization of spatial cognition would also
depend on the spatial abilities training history. At least some spatial disturbances (e.g.,
hemi-spatial neglect) have been reported to be more frequently observed associated with
left-hemisphere pathology in individuals with a history of low verbal trainings (i.e., low
educational level), but normal, and eventually even superior trainings in spatial abilities
(Rosselli et al., 1985).
________________________________________________________________
TYPE OF DISORDER
LOCATION OF DAMAGE
_______________________________________________________________
DISORDERS IN SPATIAL EXPLORATION
Balint's syndrome
Bilateral parietal-occipital
DISORDERS IN SPATIAL PERCEPTION

Inability to locate stimuli
Right parietal
Impairments in depth perception
Bilateral parietal-occipital
Distortion in line orientations
Right parietal-occipital and frontal
Inability to estimate the number of stimuli
Right hemisphere especially parietal
DISORDERS IN SPATIAL MANIPULATION

Unilateral spatial agnosia
Right occipital-parietal and frontal
Loss of topographical concepts
Parietal-temporal-occipital specially right
DISORDERS IN ORIENTATION AND SPATIAL MEMORY

Topographic agnosia
Biteral temporal-occipital
Topographic amnesia
Right (or bilateral) parietal-occipital
________________________________________________________________
Table 3.1. Classification of spatial agnosias (according to Ardila & Rosselli, 2007).
If, despite the existence of some basic characteristics in its brain organization,
language disturbances (oral and written) are associated with language idiosyncrasies (i.e.,
aphasia is not completely equivalent in Chinese and Spanish; alexia can be different in
English and Japanese, etc; Sasanuma & Fujimura, 1971; Yamadori, 1975; Yu-Huan et al,
1990), spatial cognition disturbances may also depend on spatial ability training histories.
This, of course, has to be demonstrated. And, it can be demonstrated only if spatial
disturbances are analyzed in individuals with different cultural backgrounds and different
spatial demands.
Nevertheless, contemporary city man's spatial abilities are not necessarily inferior to
pre-historical man's or Amazonian Indians' spatial abilities. Spatial abilities may have
evolved with the new living and cultural conditions (in a similar way as spoken language
evolved and extended with the development of new cultural conditions, e.g., through written
language). Spatial abilities can be required in many contemporary, conceptual, and
historically recent skills. The author of this paper had the opportunity to study a university
chemistry professor who suffered a small right-parietal infarction. Although she had no
evidence of spatial difficulty in her everyday activities, and no significant spatial
disturbances were disclosed in formal testing, she could not continue teaching chemistry,
because she was "unable to have a spatial representation of molecules and all the time got
confused". Mathematics (Ardila &Rosselli, 1990; Luria, 1977), painting, playing chess
(Chabris & Hamilton, 1992), reading and writing (Ardila & Rosselli, 1993; Benson & Ardila,
1996), mechanics (Benton, 1989), and even music (Henson, 1985), represent (at least
partially) spatially-based skills. Mathematics, painting, playing chess, reading and writing,
mechanics, and music abilities can be impaired in cases of right hemisphere damage of
those same areas that in a Eskimo or Amazonian Indian could imply an impossibility to
move around the snow or the jungle.
Neuroimaging studies
Some few studies have analyzed brain activity in different spatial recognition and
orientation tasks. Thus, by using functional Magnetic Resonance Imaging (fMRI)
techniques, it has been demonstrated that the right posterior part of the parahippocampal
gyrus is critical for the acquisition of novel information about the environment (buildings and
landscapes), and that the same region plus the anterior half of the lingual gyrus and the
adjacent fusiform gyrus play an important role in the identification of familiar buildings and
landscapes (Takahashi & Kawamura, 2002). Ino et al (2008) described two patients who
presented with transient directional disorientation as a manifestation of cerebral ischemia.
The patients suddenly lost sense of direction in a familiar environment despite preserved
ability to recognize landmarks. Brain MRI revealed an ischemic lesion in the right medial
occipital lobe and the corpus callosum in case 1 and in the right parieto-occipital sulcus in
case 2. Using a larger sample, Gil-Nciga et al. (2002) studied 10 patients with transient
topographical disorientation; they found that the episodes of transient topographical
disorientation could be separated into two types: the patients either reported difficulties in
spatial orientation with preserved abilities to recognize landmarks and objects (spatial
agnosia), or the difficulties appeared with the recognition of landmarks (topographical
agnosia). Tests exploring spatial orientation, as well as higher visuoperceptive capacities,
were altered in most of the patients, and brain SPECT showed hypoperfusion of the right
hemisphere in all patients, which could also be demonstrated two years later in some
cases.
The crucial role of the right parieto-occipital area in spatial orientation and
topographical recognition has been confirmed by diverse authors. Thus, van der Ham et al
(2010) reported two cases with navigation problems resulting from parieto-occipital right
hemisphere damage. Rusconi et al (2008) described the case of a young woman with longlasting topographical disorientation following a hemorrhagic lesion of the right temporo-
occipital region involving the hippocampus. She was unable to orient herself in novel
environments and to perform learning spatial tasks both in real-world settings and
laboratory conditions. Her ability to recall and navigate through known routes as well as to
recognize familiar landmarks was preserved. A similar neuropsychological pattern was
observed 8 years later when she showed a persistent topographical disorientation and a
slight worsening of verbal and visuo-spatial long-term memory disorders. Turriziani et al
(2003) described a patient who, following cerebral hypoxia, developed severe difficulty in
orienting himself in new environments in the context of a mild global amnesic syndrome.
Some episodes he related suggested that his main difficulty was remembering the
spatial/directional value of landmarks he recognized. A neuroradiological examination
documented severe bilateral atrophy of the hippocampi associated with atrophic changes in
the cerebral hemispheres, mostly marked in the dorsal regions.
Several notable features emerge from consideration of the case reports of relatively
pure topographical disorientation in the presence of a retrosplenial lesion (Maguire, 2001).
The majority of cases follow damage to the right retrosplenial cortex, with Brodmann's area
30 (association cortical area in the transitional region between the posterior cingulate gyrus
and the medial temporal lobe) apparently compromised in most cases. All patients
displayed impaired learning of new routes, and defective navigation in familiar
environments complaining they could not use preserved landmark recognition to aid
orientation. The deficit generally improved during the following weeks. The majority of
functional neuroimaging studies involving navigation or orientation in large-scale space also
activate the retrosplenial cortex, usually bilaterally, with good concordance in the locations
of the voxel of peak activation across studies, again with Brodmann's area 30 featuring
prominently. Currently, there is strong evidence for right medial temporal lobe involvement
in spatial orientation; it also seems that the inputs the hippocampus and related structures
receive from and convey to right retrosplenial cortex have a similar spatial preference, while
the left medial temporal and left retrosplenial cortices seem primarily concerned with more
general aspects of episodic memory.
Conclusions
Some tentative conclusions regarding the evolution of spatial abilities can be proposed:
1. Homo sapiens presented a nomad way of life during the majority of his history.
Sedentary way of life appears only with domestication of animals and development of
agriculture, that if, some ten thousand years ago. Nomad way of life is strongly associated
with high spatial ability demands.
2. Disorders in spatial cognition represent a particularly complex and insufficiently
understood array of impairments. Spatial knowledge has been strongly associated with
right hemisphere activity. Virtually all the defects in spatial perception and orientation are
found exclusively or predominantly in cases of right hemisphere damage.
3. It can be supposed that right hemisphere specialization for spatial abilities is
correlated with language acquisition and evolution. Furthermore, it has been suggested that
right hemisphere specialization on spatial skills, as well as left hemisphere specialization in
verbal and praxic abilities, is found to be correlated with literacy, that is, with language
complexization. Spoken language evolved with appearance of new cultural conditions, and
it may be supposed that spatial abilities also evolved with the appearance of new cultural
and ecological conditions.
4. It has been conjectured that earlyhominids and pre-historical man presented a
more bilateral representation of spatial abilities. Visuospatial disorders might have been
expected in cases of right and left hemisphere pathology. Not only language development
and complexization, but also the development of new spatially-based abilities may have
increased the right hemisphere specialization for handling information with a spatial
content, as well as the left specialization for linguistic abilities (LeDoux, 1984).
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Yu-Huan, H., Ying-Guan, Q., & Gui-Qing, Z .(1990) Crossed aphasia in Chinese: A clinical
survey. Brain and Language, 39, 347-356.
4. Origins of Writing
Introduction
Writing represents a relatively recent acquisition in human history. Its development was
particularly slow, advancing through different steps of complexity. Writing began several
millennia ago, but still nowadays, significant changes in writing strategies are observed very
specially associated with the progressively more extended use of computer word
processors.
The need for a clear understanding of the origins of current cognitive abilities is
evident. The example of reading and writing may be illustrative of the need for a
historical/anthropological analysis of neuropsychological syndromes. Varney (2002) points
out that reading is a cultural, not an evolutionary, development. He emphasizes that our
capacity of reading did not evolve biologically; it evolved through cultural developments that
were only acquired as typical human abilities within the last 200 years in Europe and
America, and only after World War II in the rest of the World (p. 3). The origins of reading
can be found in certain abilities that existed long before reading was developed. Reading
and writing were far from universal even at the beginning of the 21st century.
According to the United Nations, a person who is literate can, with understanding,
both read and write a short simple statement on his or her everyday life. A person is
functionally literate who can engage in all of those activities in which literacy is required for
effective function of his or her group and community and also for enabling him or her to
continue to use reading, writing, and calculation for his or her own and the communitys
development (UNESCO, 2003). Surveys throughout the world have been conducted to
observe populations speaking various languages and their inability to read or write a simple
message. In the first survey (1950), at least 44% of the worlds population was found to be
illiterate. A 1978 study showed the rate to have dropped to 32.5%. In 1990 illiteracy
worldwide dropped to about 27%, and by 1998 to 16%.
However, a study by the United Nations Childrens Fund (UNICEF) published in
1998 predicted that the world illiteracy rate would increase in the 21st century because only
a quarter of the worlds children were in school by the end of the 20th century. The highest
illiteracy rates were found in the less developed nations of Africa, Asia, and South America.
The lowest illiteracy rates were found in Australia, Japan, North Korea, and the more
technologically advanced nations of Europe and North America. Currently, there are an
estimated 862 million illiterate adults in the world, of whom about two thirds are women
(UNESCO, 2011). The mean educational level of contemporary man is only about 34
years of school!
Varney (2002) analyzed the origins of reading ability. He suggested that the ancient
skills of gesture comprehension and animal tracking were the underpinnings of brain
organization that permitted reading to occur. He demonstrated that alexia is significantly
associated with impaired pantomime and animal footprint recognition. Thus, these abilities,
existing since early human history, were prerequisites that led the way to the cultural
development of reading. Gesture recognition may have existed for several millions of years,
but reading developed just a few millennia ago.
How did writing appear?

Wall paintings appeared during the Paleolithic era, some 3035,000 years ago (Childe,
1936). Across Europe, particularly in France and Spain, cave paintings dating from the
Paleolithic age have been found. Mainly animals, but also people, instruments, and
environmental conditions, are represented in these paintings. Further evolution in pre-
writing is represented by paintings becoming standardized for representing specific

elements (i.e., a standard bird means bird). Lecours, Pea-Casanova, and Ardila (1998)
pointed out that writing began with concrete pictograms that reflect realities accessible to
the senses, particularly to vision. These pictograms further evolved and became abstract,
progressively separating from the concrete representation (Figure 4.1). This situation was
observed in Sumer (contemporary Iraq) about 53 centuries ago, and it is usually regarded
as the beginning of writing in human history. Symbols (graphemes) referred to the meaning
of the words, so these original writing systems are regarded as logographic.
Graphemes representing sounds (syllables) appeared later, about 4000 years ago in
Phoenicia (Sampson, 1985), and graphemes representing phonemes appeared even later
in Greece. The sequence of the evolution of writing in consequence was:
Drawings -> pictograms -> logograms -> syllabic graphemes -> phonemic
graphemes
Writing systems can be divided in different ways; a major distinction between

logographic (representing meanings) and sonographic (representing sounds) systems can
be established (OMNIGLOT; Sampson, 1985). The fundamental difference between
logographic writing systems and other scripts is that each logographic symbol means
something. As a result, logographic writing systems generally contain a large number of
symbols: anything from several hundred to tens of thousands. In fact there is no theoretical
upper limit to the number of symbols in some logographic scripts, such as Chinese.
Figure 4.1. Evolution from pictograms to cuneiform logograms
Logographic scripts may include the following types of symbols:

1. Logogramssymbols that represent parts of words or whole words. Some
logograms resemble the things they represent and are sometimes known as pictograms or
pictographs (Figure 4.2).
2. Ideogramssymbols that graphically represent abstract ideas.

3. Semantic-phonetic compoundssymbols that include a semantic element, which
represents or hints at the meaning of the symbol, and a phonetic element, which denotes or
hints at the pronunciation.
4. Sometimes symbols are used for their phonetic value alone, without regard for
their meaning.
In sonographic writing systems, syllables (syllabic alphabets) or phonemes
(phonemic alphabets) can be used. Alphabetic writing systems come in two varieties.
1. Abjads (consonant alphabets) represent consonants only, or consonants plus
some vowels. Even though not common, full vowel indication (vocalization) can be
added, usually by means of diacritics.
2. Alphabets (phonemic alphabets) represent consonants and vowels.
Thus, initial writing (or rather, pre-writing) was a visuoconstructive ability (i.e.,
representing external elements visually), and only later did it become an ideomotor praxis
ability (i.e., making certain learned and fixed sequences of movements with the hand to
create a pictograma standardized representation of external elements). Still later, after
writing became an ideomotor praxis ability, it became a linguistic ability (i.e., associating the
pictogram with a word, and further analyzing the word in its constituting sounds). It is not
surprising that three major disorders in writing can be observed as a result of brain
pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor (apraxic
agraphia), and linguistic (aphasic agraphia). In addition, of course, writing requires visual
and motor integrity.
Figure 4.2. Example of a logographic writing system. Japanese Kanji uses Chinese
characters that were imported from China which is use for to write nouns, adjectives,
adverbs and verbs.
It can be proposed that writing is based in three different abilities: visuoconstructive,

praxic and linguistic. Consistent with this notion, three major disorders in writing can be
observed as a result of brain injury or pathology: visuoconstructive (spatial or visuospatial
agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia) (Table 4.1).
Perhaps not coincidentally, anthropological origins of writing appear to mirror these three
different abilities. In prehistory, writing developed first using a visuospatial modality to
create three-dimensional clay tokens to represent objects, which later progressed into
drawings. It is not surprising that three major disorders in writing can be observed as a
result of brain pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor
(apraxic agraphia), and linguistic (aphasic agraphia). In addition, of course, writing requires
visual and motor integrity.
--------------------------------------------------------------------------Spatial or visuospatial agraphia

Apraxic agraphia
Aphasic or linguistic or central agraphia
--------------------------------------------------------------------------Table 4.1. There are three fundamental forms of agraphia (Ardila, 2004).
How many people can write?

Even though writing began several millennia ago up to as recently as the 1950s, about half
of the worlds population was illiterate. The percentage of illiteracy dramatically increases
as we go back in time, and up to only a couple of centuries ago, the overwhelming majority
were illiterate. Until the 15th century, when the printing press was invented, writing may well
have been limited to a few intellectual people and monks. Even though there are no
statistics available, it may be conjectured that 99% or more of the population was illiterate.
Furthermore, it has to be kept in mind that the mean level of education of contemporary
man is about 3 years of school, which may not be enough to develop automatic reading
and writing.
It is evident that writing represents an unusual ability in humans. The overwhelming
majority of members of our species who have lived could not read or write. Reading and
writing is obviously far from being a primary or biologically based cognitive ability.
Clearly, writing represents a cognitive ability that depends on the human cultural evolution
(Vygotsky, 1962).
Agraphia as a neuropsychological syndrome

Agraphia can be defined as the partial or total loss of the ability to produce written language
and is associated with brain pathology. The ability to write can be impaired as a result of
linguistic defects (aphasia), but other elements not related to language (e.g., motor and
spatial) also participate in the writing ability. It supposes knowledge of the language codes
(phonemes, words), an ability to convert language sounds in graphemes, knowledge of the
graphemic system (alphabet), an ability to perform fine movements, and an appropriate use
of the space for distributing, joining, and separating letters. It is evident that diverse types of
writing disturbances can be found in clinical practice.
Different attempts to classify writing disturbances are found in the history of
neuropsychology. Goldstein (1948) distinguished two major types of agraphia:
apractoamnesic and aphasic-amnesic. Luria (1976, 1980) referred to five different types of
agraphia, three of them associated with aphasia (sensory agraphia, afferent motor
agraphia, and kinetic agraphia) and two associated with visuospatial defects. Hecaen and
Albert (1978) distinguished four types of agraphia: pure, apraxic, spatial, and aphasic.
Regardless of the diversity of classifications of agraphia, a basic distinction can be
established between (1) agraphias due to a language impairment (linguistic or aphasic
agraphias), (2) agraphias due to other types of impairments (most often, motor or spatial)
disturbing the normal ability to write (Benson & Ardila, 1996), or simply (3) central and
peripheral agraphias (Ellis, 1988). In the first case, agraphia is just a secondary
manifestation of the aphasic syndrome. In the second, it can be interpreted as a result of a
broader visuoconstructive/visuospatial impairment (Ardila & Rosselli, 1993), or motorapraxic disturbance (Hecaen & Albert, 1978). Consequently, writing can be interpreted as a
particular type of cross-modal learning. Certain visuoconstructive and ideomotor abilities
become associated with language.
It can be proposed that writing is based in three different abilities: visuoconstructive,

praxic and linguistic. Consistent with this notion, three major disorders in writing can be
observed as a result of brain injury or pathology: visuoconstructive (spatial or visuospatial
agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia). Perhaps not
coincidentally, anthropological origins of writing appear to mirror these three different
abilities. In prehistory, writing developed first using a visuospatial modality to create threedimensional clay tokens to represent objects, which later progressed into drawings.
Dysexecutive agraphia
Regardless that many types of writing disorders associated with brain pathology have been
described throughout the history, limited mention to the writing disturbances associated
with prefrontal pathology, however, is found. Clinical observations of patients not only with
focal prefrontal pathology but also with other conditions affecting the frontal lobe system
(e.g., traumatic head injury, dementia) confirm the assumption that these patients present
an overt decrease in the ability to express ideas in writing. It can be argued that complex
aspects of writing, such as planning, narrative coherence, and maintained attention, are
significantly disturbed in cases of impairments of executive functions (dysexecutive
syndrome). Frontal lobe patients not only have difficulties in keeping the effort required for
writing, but also to organize the ideas in the written texts. The term dysexecutive agraphia
(Ardila & Surloff, 2006) has been proposed to refer to this writing disorder.
Is any area in the brain specialized for writing?

Writing is a functional system (Luria, 1976) that requires, and is based on, some more
fundamental abilities: praxis abilities (i.e., learning sequences of movements required to
write the letters), spatial abilities (distributing letters and words in the space, and
understanding the value of space in writing), constructional abilities (reproducing a model

using certain movements), and obviously, the knowledge of the language and the
association between verbal auditory elements and visual symbols. Varney (2002) refers to
the anthropological concept of pre-adaptation, which states that the evolution of a structure
for one purpose can enable that structure to perform another purpose.
This must be true for writing (as for any other abilities depending on cultural
evolution). Visuoconstructive and ideomotor abilities represent prerequisites for writing;
they are probably related to the ability to make tools and weapons and generally to use the
hands in a skilled way.
Brain activation during writing

The use of contemporary neuroimagening techniques has significantly advanced the
understanding of the brain organization of writing (see www.fmriconsulting.com/
brodmann/). It has been observed that writing is associated with an extended pattern of
brain activity, usually including a diversity of anterior and posterior, right and left areas.
Indeed, writing is a complex act, requiring not only linguistic but also motor and spatial
abilities.
Functional studies have demonstrated that writing single letters is associated with a
significant activity of Brodmanns areas 37 (temporal-occipital area, related with auditoryvisual associations) and 7 (superior parietal lobe) (Rektor et al., 2006). Other parietal areas
are also active during writing including the border between the parietal superior and inferior
lobuli Brodmanns area (Brodmanns areas 2 and 40), deep in the intraparietal sulcus, with
a surprising right-sided dominance. The right parietal activation may reflect the spatial
dimension of writing.
Comparing the brain activity observed during writing and drawing a relatively similar
pattern of activation for both has been reported (Harrington et al., 2007) including bilaterally
the premotor, inferior frontal, posterior inferior temporal and parietal areas. Significant
differences between the two conditions (writing and drawing) are found in areas of the brain
known for language processing (perisylvian area); greater activation for writing is observed
in the left hemispheres, whereas greater right hemisphere activation for drawing is found in
homologous areas, particularly Brodmanns area 46 (part of the prefrontal cortex - anterior
middle frontal gyrus) and 37 (temporal-occipital).
Sugihara et al. (2006) recorded the brain activation while writing with the right and
the left hand using Japanese Kana (phonograms representing syllables). Three areas
were found to be activated: (1) the posterior end of the left superior frontal gyrus, which is
superior and posterior to the so-called Exner's area (an area just above Broca's area and
anterior to the primary motor control area, initially described as the writing center); (2) the
anterior part of the left superior parietal lobule; and (3) the lower part of the anterior limb of
the left supramarginal gyrus. In the single-subject analysis, whereas the first two of the
above three areas were found to be crucial for writing in all individuals, an interindividual
inconsistency of involvement with writing was observed in last area: the lower part of the
anterior limb of the left supramarginal gyrus (60% involved); the right frontal region (47%);
and the right intraparietal sulcus (47%).
Writing in different systems

Few papers have approached the question of the potential similarities and differences in
agraphia clinical manifestations across different writing systems. Some studies have
approached the comparison of writing disturbances and brain activation patterns in
Japanese Kana and Kanji. More recently, studies of agraphia in other languages have
become available.
Indeed, Japanese represents a unique language using two different writing systems;
Kana is a phonographic system and symbols represents syllables; whereas Kanji is a
logographic system and symbols represent meanings (morphograms). Various types of

alexia with or without agraphia in the Japanese language cause specific type of Kanji/Kana
dissociation; it has been further proposed that there is a semantic reading pathway via
Brodmanns area 37 on the inferior border of the left temporal lobe and a phonological
reading pathway via middle portion of the left lateral occipital lobe (Iwata, 2004)
Yaguchi et al. (2006) reported a case of pure (apraxic) agraphia observed both in
Kana and Kanji writing to dictation and copying. Most errors in Kana and Kanji writing to
dictation and copying were no response. The patient, however, was able to write numerals
from 1 to 12 precisely. Magnetic resonance imaging showed a cerebral infarction in the left
parietal lobe which included a part of superior parietal lobule and supramarginal gyrus. That
means the apraxic agraphia was similarly affecting both writing systems Kana and Kanji.
Sakurai et al. (2008) analyzed two patients with lesions of the left posterior middle
temporal gyrus. Patient 1 first presented with pure alexia more impaired for Kana after an
infarction in the left middle and inferior occipital gyri and right basal occipital cortex, and
after a second infarction in the left posterior middle temporal gyrus adjoining the first lesion
he showed alexia with agraphia for Kanji and worsened alexia for Kana; Kanji alexia
recovered over the following six to 10 months. Patient 2 presented with alexia with agraphia
for Kanji following a hemorrhage in the left posterior middle and inferior temporal gyri, which
resolved to agraphia for Kanji at two months after onset. In both patients, Kanji agraphia
was mostly due to impaired character recall. The authors concluded that damage to the left
posterior middle temporal gyrus alone can cause agraphia for Kanji. If the adjacent mid
fusiform/inferior temporal gyri (Brodmanns area 37) are spared, the Kanji alexia is
transient. This report also demonstrates that agraphia for Kana and for Kanji can be at least
partially dissociated.
Ihori et al. (2006) reported the case of a right-handed patient who exhibited right
unilateral jargonagraphia after a traumatic callosal hemorrhage. The lesions involved the
entire corpus callosum, except for the lower part of the genu and the splenium. The
patient's right unilateral jargonagraphia was characterized by neologisms and perseveration
in Kanji and Kana, and was more prominent in Kana than Kanji. The authors propose that
at least two factors seem to explain that Kana was more defective than Kanji. First, writing
in Kana, which is assumed to be processed mainly via a sub-word phoneme to grapheme
conversion route, might depend more strongly on lateralized linguistic processing than
writing in kanji. Second, kanji, which represent meaning as well as phonology, with much
more complicated graphic patterns than kana, are assumed to be processed in both
hemispheres.
Fukui and Lee (2008) reported three patients with progressive agraphia; initially,
these patients complained primarily of difficulties writing Kanji while other language and
cognitive impairments were relatively milder. It was proposed that agraphia was generally
more prominent, although not exclusive, for Kanji, probably because of later acquisition and
larger total number of Kanji symbols leading to lower frequency of use and familiarity per
symbol. For comparing purpose, it is worthy to mention the case of progressive agraphia in
a Spanish speaking woman reported by Ardila et al., (2003). This patient presented a
progressive deterioration of writing abilities, associated with acalculia and anomia. An MRI
disclosed a left parietal-temporal atrophy. Using Spanish orthography was the initial writing
difficulty noted in this woman. The correct use of orthography (i.e., selecting between two
or more homophone alternatives) represents for normal people the most difficult aspect in
Spanish writing, and it is not surprising to find it was the most fragile writing ability in this
patient. In a further evaluation two years after the initial symptomatology, the patient
demonstrated not only orthographic (homophone) errors, but also letter omissions and
additions, and even non homophone errors. It is noteworthy that, regardless of her inability
to write spontaneously or by dictation, her writing by copy was virtually perfect. It was
conjectured that writing by copy does not really represent a linguistic ability but rather
visuoperceptual and visuoconstructive ability.
Lin et al. (2007) using fMRI examined the neural correlates for Chinese writing, by
comparing the writing of logographic characters and that of pinyin, a phonetic notation
system for Chinese characters. The temporal profile of the activations indicated that the
middle frontal gyrus, superior parietal lobule, and posterior inferior temporal gyrus reflected
more central processes for writing. Although pinyin writing elicited greater activity overall
than character writing, the critical finding was that the two types of symbols recruited
essentially the same brain regions. Liu et al. (2007) trained native English speakers with no
knowledge of Chinese on 60 Chinese characters. Following the training, fMRI scans taken
during passive viewing of Chinese characters showed activation in brain regions that
partially overlap the regions found in studies of skilled Chinese readers, but typically not
found in alphabetic readers. Areas include bilateral middle frontal (Brodmanns area 9),
right occipital (Brodmanns area 18/19), and fusiform (Brodmanns area 37) regions. The
results suggest that learners acquired skill in reading Chinese characters using a brain
network similar to that used by Chinese native speakers.
Meschyan and Hernandez (2006) compared the pattern of brain activation during
single word reading in a group of English/Spanish bilinguals. Participants were slower in
reading words in their less proficient language (Spanish) than in their more proficient
language (English). fMRI revealed that reading words in the less proficient language
yielded greater activity in the articulatory motor system, consisting of supplementary motor
area/cingulate, insula, and putamen. Orthographic transparency also played a
neuromodulatory role. More transparent Spanish words yielded greater activity in superior
temporal gyrus (Brodmanns area 22), a region implicated in phonological processing, and
orthographically opaque English words yielded greater activity in visual processing and
word recoding regions, such as the occipital-parietal border and inferior parietal lobe
(Brodmanns area 40).
From agraphia to dystypia

Contemporary literate man is using handwriting less and less, and relying on computers
more and more. In an informal survey of 40 people with a college-level education
background, they reported using a computer about 90% of the time when writing and
handwrote only 10% of the time. Obviously, this sample does not represent all of
humankind, and computers are not accessible to a large percentage of the human
population. But this sample seems to illustrate the way in which writing is evolving: from
handwriting to typing on a computer.
Handwriting and using computers represent significantly different cognitive and
motor abilities. During handwriting, fingers are maintained in a relatively steady position
while the hand moves. In typing, the opposite pattern is observed. When typing, the right
hand does not move from one side to the other and back as in handwriting, but the hands
remain relatively stationary and only the fingers are moved. Letters are not written but
selected. Both hands have to be used in a similar way when typing. Because of using both
hands, we have to assume that a major interhemispheric integration is required. It is
obvious to assume that right-hemisphere lesions located in the frontal and parietal areas
should significantly impair the typewriting ability of the left hand. Similarly, the use of the
space is different.
The normal spatial distribution of the words on the page is automatic on the
computer and, hence, writing in this way cannot be spatially disorganized, which may be
the case in handwriting. By the same token, letters are neatly written and easily
recognizable. When typing, we are not using a space that is directly manipulated with the
hands (constructional space), but only a visual space. Furthermore, typing is not a
constructional task (we do not have to construct the letters) but rather a motor-spatial task.
Many people type using a spatial memory for the position of the letters in the keyboard.
This is a type of memory not required in handwriting, and it probably depends on right
hippocampal and parietal activity (Moser, Hollup, & Moser, 2002). Other people have to
look at the keys to select the letters when typing. In this case, literal reading is a
prerequisite for writing. Letters have to be recognized visually before they are written. In
handwriting, we use a mental representation of the visual form of the letters. Interestingly,
few peopleif any, regardless of how well they can typeare able to reproduce (i.e.,
describe verbally or by drawing) how the different letters are arranged on the keyboard.
Memory for their location seems to be a purely spatial and motor memory of which we are
poorly aware.
For typing some special symbols (e.g., interrogation marks) and letters (the Spanish
N ), some relatively sophisticated motor maneuvers are required, sometimes requiring the
use of special keys or sequences of movements. In handwriting, however, special symbols
are written using the mental forms that we have learned. When typing, if a letter needs to
be lower or upper case, a key has to be pushed. No other change to the movement is
made. We can also select different writing styles and letter sizes using some special
commands and menus, all without changing the sequences of the hand movements. In
cases of brain damage, how is typewriting altered? To the best of my knowledge, only one
case of agraphia for typewriting has been published (Otsuki, Soma, Arihiro, Watanabe,
Moriwaki, & Naritomi, 2002). Nonetheless, it can be assumed that different types of brain
pathology may affect the ability for typing on a computer word processor. The following can
be conjectured.
1. An anterior callosal lesion would impair the ability to coordinate the movements
between the hands. Furthermore, the left hand would be isolated from the linguistic left
hemisphere and would be unable to write. Left-hand hemiagraphia in callosal lesions has
been observed (Benson & Ardila, 1996).
2. By the same token, it has been observed that damage in the supplementary motor
area results in disturbances in the coordinated movements between both hands (Middleton
& Strick, 2001). We can anticipate supplementary motor area typing agraphia.
3. Spatial memory disturbances should result in difficulties in recalling the positions
of the letters on the keyboard. Typing would be slow and would require a continual search
for the letters.
Otsuki et al. (2002) reported on a 60-year-old right-handed Japanese man who
showed an isolated persistent typing impairment without aphasia, agraphia, apraxia, or any
other neuropsychological deficit. They proposed the term dystypia for this peculiar
neuropsychological manifestation. The symptom was caused by an infarction in the left
frontal lobe involving the foot of the second frontal convolution and the frontal operculum.
The patients typing impairment was not attributable to a disturbance of the linguistic
process, since he had no aphasia or agraphia. Nor was it attributable to an impairment of
the motor execution process, since he had no apraxia. Thus, it was deduced that his typing
impairment was based on a disturbance of the intermediate process where the linguistic
phonological information is converted into the corresponding performance. The authors
hypothesized that the foot of the left second frontal convolution and the operculum may
play an important role in the manifestation of dystypia.
Using a computer is somehow equivalent to a new writing system. Obviously,
there is no brain area related to typing on a computer, as there is no brain area related to
reading and writing. These are cultural and technological elements recently developed
through human evolution. However, there are basic cognitive abilities (pre-adaptative
abilities) that are required for the use of these new cultural elements: e.g., certain
visuoperceptual abilities and cross-modal associations for reading, phonological awareness
and some fine movements for writing, etc. Using computers is notoriously more complex,
yet we can assume a functional system participating in their use.
It can be conjectured that using computers requires at least the following abilities:
1. A conceptual ability (executive functioning) to understand the principles governing
the functioning of a computer.
2. Some visuoperceptual abilities to recognize icons, windows, etc.
3. Some skilled movements to type on the keyboard and manoeuvre the mouse
correctly.
4. Some spatial abilities to handle the working space (monitor screen).
5. Some memory abilities to learn programs, to use the spatial position of the keys,
etc.
Obviously, the ability to use computers can potentially be disrupted as a
consequence of a failure in any one of these abilities (acumputuria syndrome). In the
future, apart from dystypia, more complex disturbances in the ability to use computers will
probably be established.
Conclusions
The origins of writing can be traced back to cave paintings. Writing (or pre-writing) was
initially a visuoconstructive ability, later involving some stereotyped movements to
represent pictograms, and finally involving spoken language. It makes sense, therefore,
that
the
ability
to
write
can
be
disturbed
in
three
major
forms:
as
visuospatial/visuoconstructive dexterity, as an ideomotor skill, and as a linguistic ability.

Writing has followed a long evolution since cave painting during the Palaeolithic times.
Different strategies have been used to represent spoken language visually
(ideograms, alphabets, etc). Writing, however, has continued to evolve since its initial
invention. The use of punctuation marks and the distinction between upper and lower case
in writingto mention just two examplesare relatively recent in history (Sampson, 1985).
Evolution has continued with the development of different technical instruments for writing:
the feather, the pencil, the typewriter, and the computer. Brain representation of written
language has necessarily changed in some way, too. Neuropsychological syndromes
associated with brain pathology have evolved over time.
We can assume that the consequences of brain pathology in a Palaeolithic man
were not the same as for a 19th-century individual (when agraphia was first described), or
for contemporary man or woman (some of whom frequently spending most of their working
day in front of a computer screen). It can be anticipated that in the future new
neuropsychological syndromes resulting from new living conditions will be described.
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5. Origins of Calculation Abilities2
Introduction
Calculation ability represents an extremely complex cognitive process. It has been
understood to represent a multifactor skill, including verbal, spatial, memory, and executive
function abilities (Ardila et al., 1998). Calculation ability is quite frequently impaired in cases
of focal brain pathology (Ardila & Rosselli, 2002; Dansilio, 2008; Domahs et al., 2011;
Grafman, 1988; Hecaen et al., 1961) and dementia (Deloche et al., 1995; Grafman et al.,
1989; Parlatto et al., 1992; Rosselli & Ardila, 1998). The loss of the ability to perform
calculation tasks resulting from a cerebral pathology is known as acalculia or acquired
dyscalculia. Acalculia has been defined as an acquired disturbance in computational ability
(Loring, 1999). The developmental defect in the acquisition of numerical abilities, on the
other hand, is usually referred to as developmental dyscalculia or dyscalculia.
Calculation abilities have followed a long process from the initial quantification
systems up to modern algebra, geometryy, and physics. Some rudimentary numerical
concepts are observed in animals, and there is no question that pre-historic man used
some quantification. However, the ability to represent quantities, the development of a
numerical system, and the use of arithmetical operations are found only in old civilizations.
This chapter reviews the evolution of calculation abilities, including numerosity and
counting in non-human animals, calculation abilities in primitive and modern humans, and
links between language and number concepts throughout human history. In addition, the
paper reviews contemporary studies of the neurological substrates of numerical abilities
and discusses the implications of technological advances with regard to continued evolution
of these abilities.
1. A previous version of this paper was published in: Ardila, A. On the evolution of calculation abilities. Frontier in
Evolutionary Neurosciences, 2, 1-8.
Numerical concepts in animals

The origin of mathematical concepts can be traced to sub-human species. Throughout
recent history different reports have argued that animals (horses, rats, dogs, chimpanzees,
dolphins, and even birds) can use numerical concepts and perform arithmetical operations.
Some of these reports represent evident charlatanry directed to the general public. Some
others, however, are rigorous and highly controlled scientific studies (e.g., Rugani et al.,
2009).
There is, in general, agreement that some rudimentary numerical concepts are
observed in animals. These basic numerical skills can be considered as the real origin of
the calculation abilities found in contemporary man. For instance, pigeons can be trained to
peck a specific number of times on a board, and rats can be trained to press a lever a
certain amount of times to obtain food (Koehler, 1951; Mechner, 1958; Capaldi & Miller,
1988). It could be conjectured that pigeons and rats can count, at least up to a certain
quantity; that is, they can recognize how many times a motor act to peck on a board or to
press a lever has been repeated. Whether or not this behavior can really be interpreted
as counting is nonetheless questionable. However, this behavior can be observed after
long and painstaking training. Nonetheless, these animal responses (to peck or to press the
lever) are not precise but just approximate. In other words, when the rat is required to press
the lever seven times, the rat presses it about seven times (i.e., 5, 6, 7, 8 times). As
Dehaene (1997) emphasizes, for an animal, 5 plus 5 does not make 10, but only about 10.
According to him, such fuzziness in the internal representation of numbers prevents the
emergence of exact numerical arithmetical knowledge in animals. Using highly controlled
and sophisticated designs, it has been pointed out that chimpanzees can even use and add
simple numerical fractions (e.g., 1/2 + 1/4 = 3/4) (Woodruff & Premack, 1981). These
observations support the assumption that some quantity concepts can be found in different
animals.
Counting (or rather, approximately counting) motor responses is a motor act as is

walking or running. Counting lever pressings is not very different from estimating the effort
(e.g., number of steps or general motor activity) required in going from one point to another.
Counting in such a case could be linked to some proprioceptive and kinesthetic information.
In the human brain Kansaku et al. (2006) identified a network of areas involved in
enumerating small numbers of auditory, visual, and somatosensory stimuli, and in
enumerating sequential movements of hands and feet, in the bilateral premotor cortex, presupplementary motor area, posterior temporal cortex, and thalamus. The most significant
consistent activation across sensory and motor counting conditions was observed in the
lateral premotor cortex. Lateral premotor activation was not dependent on movement
preparation, stimulus presentation timing, or number word verbalization. Furthermore,
movement counting, but not sensory counting, activated the anterior parietal cortex.
Chimpanzees, but also rats and many other animals, can distinguish numerosity
(i.e., global quantification); for instance, they prefer a bowl containing a larger number of
nutritive elements (such as chocolates or pellets) when selecting between two bowls
containing different amounts (Davis & Perusse, 1988). It may be conjectured that global
quantification (numerosity perception) and counting (at least the approximate counting of
motor responses) represent kinds of basic calculation abilities found at the animal level.
Rats prefer a bowl containing 20 pellets to a bowl containing only 10 pellets; however, they
do not prefer a bowl containing 20 pellets to a bowl containing 21 pellets. Obviously,
numerosity perception is related to the size and shape of the visual image projected to the
retina. It can be assumed that 20 pellets in a bowl result in a larger and more complex
retinal image than 10 pellets. But the visual image corresponding to 20 pellets is difficult to
distinguish from the visual image corresponding to 21 pellets.
Development of calculation abilities in children
During child development, different stages in the acquisition of numerical knowledge are
observed (Klein & Starkey, 1987). They include global quantification, recognition of small
quantities, numeration, correspondence construction, counting, and arithmetic (Table 5.1).
As mentioned, some fundamental numerical concepts can be observed at the animal level,
and it is not surprising to find them in small children. The initial levels of numerical
knowledge are found in pre-school children. The development of complex numerical
concepts requires long school training. Complex arithmetical concepts depend upon a
painstaking learning process, and they are not usually found in illiterate people. The
different stages in the acquisition of numerical concepts are associated with the language,
perceptual, and general cognitive development. Variability is normally observed, and some
children can be faster in the acquisition of numerical abilities. The different stages appear in
a sequential way, and the understanding of more complex concepts requires the acquisition
of more basic levels. A percentage of otherwise normal children can fail in using numerical
concepts normally expected at their age. The term developmental dyscalculia has been
used to refer to this group of underperforming children.
Numerical abilities in pre-school children

Global quantification or numerosity perception represents the most elementary
quantification process. Global quantification supposes the discrimination between
collections containing different number of objects (Davis et al., 1985). Global quantification
simply means which set of elements is bigger and which one is smaller. Global
quantification is observed at the animal level: Many animals can select the larger collection
of elements when they have to choose. However, the ability to distinguish which collection
is larger depends upon the number of elements in the collections. To distinguish 3 and 4
elements may be easy (4 is 25% larger than 3). To distinguish 10 and 11 elements is
obviously harder (11 is only 10% larger than 10). By the same token, to distinguish 10 from
20 elements is easy (the double), but to distinguish 100 from 110 is hard (one tenth). What
is important is the ratio existing between the two collections of elements (so called
psychophysics Weber's fraction).
__________________________________________________________________________________
Global quantification
What collection is bigger and smaller
Recognition small quantities
Differentiate one, two and three elements
Enumeration
Sequencing the elements in a collection
Correspondence construction
To compare collections.
Counting
A unique number name is paired with each object
one-one principle
Each object in a collection is to be paired with one and only one

number name
stable order principle
Each name is assigned to a permanent ordinal position in the list
cardinal principle
The final number name used in a counting sequence refers to the

cardinal value of the sequence
Arithmetic
Number permutability (e.g., adding, subtracting).
__________________________________________________________________________________
Table 5.1. Different levels of numerical knowledge (adapted from Klein and Starkey,
1987)
Global quantification is expressed in the language with words such a "many", "a lot"
and similar terms. For small quantities, the words "several", "a few" and similar quantity
adverbs are included in the language. Quantity adverbs used in everyday speech represent
global quantifiers. Quantity adverbs appear early in language history and also in child
language development earlier than the numerical system. As mentioned before, all known
world languages use global quantification and possess words to refer to many, a lot. All
languages oppose small quantities (one, two, a few) to many, a lot. As a matter of fact,
many, much and similar global quantifiers represent early words in language
development.
Global quantification, however, does not represent a truly numerical process
because it does not suppose a one-to-one correspondence. Enumeration (sequencing the
elements in a collection of elements; this process supposes the individualization of each
element) represents the most elementary type of true numerical knowledge (Klein &
Starkey, 1987). Enumeration is required to distinguish the individual elements in the
collection (this, this, and this, etc). In child language development, the most elementary
distinction is between this and other. This and other are also early words in child
language development.
Correspondence construction constitutes a type of enumeration used to represent
the number of objects in a collection and to compare collections. The amount of elements
in a collection is matched with the amount of elements in an external aid (fingers, pebbles,
knots, strokes, marks, dots, etc.). It implies, in consequence, a one-to-one correspondence:
Each one of the elements in the collection corresponds to one finger, or pebble, knot,
stroke, mark, or dot, or whatever. An external devise can be used for making the
correspondence construction. The most immediate devise are the fingers. During
enumeration usually the fingers are used to point the objects.
Counting represents a sophisticated form of enumeration: a unique number name is
paired with each object in a collection, and the final number name that is used stands for
the cardinal value of that collection. The initial object that is pointed to corresponds to
one, the following to two and so on. Some times, the very same finger name is used as
number name (i.e., the very same word is used for one and thumb, two and index finger,
etc.). The collection has the amount of objects that corresponds to the last pointed object
(cardinal principle). Arithmetic represents an advanced numerical system, which comprises
number permutability (e.g., adding, subtracting).
Human infants are able to recognize numerosity for small quantities (usually up to
three-six items) (Antell & Keating, 1983), but the ability to construct correspondences
emerges only during the child's second year (Langer, 1986). During the second year the
child also begins to use some number name, and usually develops the ability to correctly
count up to three. The child thus acquires the knowledge of two basic principles in counting.
(1) One-to-one principle (i.e., each object in a collection is to be paired with one and only
one number name). (2) The stable order principle (each name is assigned to a permanent
ordinal position in the list; the sequence of numbers is always the very same: one, two,
three, etc.). At this point, however, the child does not yet exhibit a cardinal principle; i.e.,
the final number name used in a counting sequence refers to the cardinal value of the
sequence. If a collection is counted one, two, three, it means that in that collection there
are three objects) (Klein & Starkey, 1987). Cardinal principle will be observed in
three-year-old children (Gelman & Meck, 1983).
At this point, the child can count small quantities, usually below 10. During this
period the child is also learning how the numerical system works and memorizing the
number words. Most often, the numerical system contains three different segments: (1)
from one to ten different words are used. (2) From 10 to 20 counting becomes idiosyncratic
and quite frequently irregular. In English eleven has not any apparent relationship with
one; twelve has an evident relation with two but it is a unique word number; from 13 to
19 the ending teen is used. In Spanish, from 11 (once) to 15 (quince) the ending ce is
used. From 15 to 19 the words numbers are formed as ten and six, ten and seven etc.
20 (veinte) has not any apparent relation with 2 (dos). And (3) from 20 on the numerical
system becomes regular. Word numbers are formed as twenty and one, twenty and two,
etc. Learning of the whole numerical system usually is completed at school.
Computational strategies (e.g., adding; if a new item is included in a collection, the

collection will become larger and the next cardinal number-name will be given to that
collection) are found in three-to five-year-old children, initially only for small quantities.
Development of numerical abilities at school

Adding and subtracting numerical quantities and the use of computational principles are
observed during in first-and-second grade children, but they only become able to
manipulate the principles of multiplying and dividing after a long and painstaking training
period, usually during third to fifth grade.
Understanding that subtracting is the inverse operation of adding is usually acquired
at about five to six years of age. At this age the child begins to use three different
procedures for performing additions and subtractions: (1) Counting using the fingers. (2)
Counting aloud not using the fingers. And, (3) memorizing additions and subtractions for
small quantities (one plus one is two; two plus two is four; two minus one is one, etc.). The
last strategy becomes progressively stronger when advancing age and schooling.
Nonetheless, children continue using the finger for adding and subtracting larger quantities.
From the age of 10 until about 13 years, counting using the fingers progressively
disappears, but counting aloud, and performing arithmetical operations aloud, remains.
Automatic memory not only for additions and subtractions, but also multiplications
(multiplication tables) and divisions, becomes progressively more important. (Siegler, 1987;
Grafman, 1988). As a matter of fact, adding and subtracting one digit quantities (e.g., 7 + 5
= 12; 4 + 5 = 9; 8 5 = 3; etc.) represents a type of numerical rote learning, similar to the
multiplication tables. Interesting to note, the performance of arithmetical operations aloud
may remain during adulthood, even in highly educated people.
It should be emphasized that there is a significant variability in the specific strategies
used by different children at the same age. Furthermore, the very same child can recur to
different strategies when solving different arithmetical problems. In some situations, for
instance, the child can recur to the fingers, whereas in a different operation, it may not
require using the fingers. Or, the child can be able to use some multiplication tables
whereas failing with others.
At about the age of eight to nine the children usually learn to multiply. This requires
the memorization of the multiplication tables. The errors most frequently found when
learning the multiplication tables are those answers that could be correct for other number
within the same series (e.g., 4 X 5 = 16). These errors may be the result of some
interference. They can be observed in children at any age, and even they are some times
found in normal adults (Graham, 1987).
Development of abstract reasoning and increase in working memory span contribute
to the use of mathematical algorithms, i.e., the set of rules used for solving arithmetical
problems following a minimal number of steps. The development of algorithms begins when
learning the basic arithmetical operations. Progressively, they become more automatic,
representing basic strategies for solving arithmetical problems. Development of abstract
thinking allows for the use of magnitudes to be applied to different systems (use of the
numerical system in measuring time, temperature, etc.) and to the understanding of
quantities expressed in a symbolic way
Calculation abilities in pre-historic man

Chimpanzees are capable of various forms of numerical competence, including some
correspondence constructions (that is, comparing two collections of elements) for low
quantities (Premack, 1976; Davis & Perusse, 1988). Most likely, these numerical abilities
also existed in pre-historic man. Homo sapiens antecessors may have been capable of
using correspondence constructions in some social activities, such as food sharing. It has
been proposed that Homo habilis (ancestor of Homo erectus, living about 2.3 million to 1.4
million years ago) needed to use correspondence constructions when butchering large
animal carcasses (Parker & Gibson, 1979). Distributing pieces of a divided whole (e.g.,
prey) into equal parts required the ability to construct one-to-one correspondences.
Paleolithic man was probably able to match the number of objects in different groups and,
eventually, the number of objects in a collection with the number of items in some external
cue system, e.g., fingers or pebbles (incidentally, calculus means pebbles).
The immediate recognition of certain small quantities is found not only in animals,
but also in small children. Animals and children can readily distinguish one, two, or three
objects (Fuson, 1988; Wynn, 1990, 1992; Cook & Cook, 2009). Antell and Keating (1983)
observed that newborn infants were able to discriminate among visual stimulus arrays
consisting of a few dots. It was found that infants were able to discriminate between small
numbers (2 versus 3) but not for larger sets. This ability for discriminating and also
representing and remembering small numbers of items has also been reported by other
authors (e.g., Starkey & Cooper, 1980). Interestingly, evoked potentials at three months are
already capable of marking changes in the nature and number of a set of objects, and
these activation changes relate to the parietal lobe (Dehaene & Dehaene-Lambertz, 2009).
Noteworthy, in normally developing children and adults, the increase in arithmetic
competence is associated with shift of activation from frontal brain areas to parietal areas.
A shift of activation is also observed within the parietal lobe from the intraparietal sulci to
the left angular gyrus; experts arithmetic proficiency depends on a more extended
activation than the network found in beginners. In expert individuals with solid, extensive
mathematical training, specific brain activation changes are also observed (Zamarian et al.,
2009).
Oneness, twoness, and threeness seemingly are basic perceptual qualities that our
brain can distinguish and process without counting. It can be conjectured that when prehistoric humans began to speak, they may have been able to name only the numbers one,
two, and three, corresponding to specific perceptions. To name them was probably no
more difficult than naming any other sensory attribute (Dehaene, 1997). Of note, all world
languages can count up to three, even though three may represent many, several, or a
lot (Hurford, 1987). One is obviously the unit, the individual (the speaker may also be
one). Two conveys the meaning of another (for example, in English and also in
Spanish, second is related with the verb to second and the adjective secondary).
Three may be a residual form of a lot, beyond the others, or many (for example,
troppo, which in Italian means too much, is seemingly related with the word three -tre).
In the original Indo-European language, spoken perhaps some 1500020000 years ago,
apparently the only numbers were one, one and another (two), and a lot, several, or
many (three) (Dehaene, 1997). Interestingly, in some contemporary languages, two
different plurals are found: a plural for small quantities (usually two, sometimes three and
four) and a second plural for larger quantities; for instance, in Russian, one house is odin
dom, two, three, or four houses is dva, tri, cheterye doma but five houses is pyat
domov.
Of note, in different world languages, the word one does not have any apparent
relationship with the word first; and the word two is also not related with the word
second. Three may sometimes, but not always, hold some relationship with third.
Beyond three, ordinals are clearly associated with cardinal numbers (Table 5.2). The conclusion is obvious: for small quantities (one, two, three), cardinals and ordinals must have a
different origin. For larger quantities, ordinal numbers are derived from cardinals. As a
matter of fact, one/first and two/second correspond to different conceptual categories.
It may be speculated that for pre-historic man the first person and the second person
in a line (or the first animal and the second animal during hunting, or other similar concepts)
do not seem to be related with the number one and the number two. For small children
first has the meaning of initial (e.g., I go first) whereas second is related to later or
after (e.g., you go second). These words have a temporal and also spatial meaning, but
not an evident numerical meaning. The association between one and first, and two and
second seems a relatively advanced process in the development of numerical concepts.
That is, the numerical meaning of first and second seems to appear after its temporal
and spatial meaning. The association between ordinals and cardinals becomes evident only
for larger quantities (more than three) and seems to represent a later acquisition in human
evolution and the complexization of numerical concepts. Moreover, in many contemporary
languages (e.g., the Huitoto language, spoken by the Huitoto Indians in the Amazonian
jungle; indian-cultures.com/ Cultures/huitoto.html) there are no ordinal numbers. For first,

the Huitoto language uses the beginning; to express second the word another is used.
____________________________________________________________________________________
English Spanish Russian
Greek Persian
Arab
Hindi
Aymara(1)
Ibo (2)
____________________________________________________________________________________
One
Uno
Odin
Ena
Yek
Wahid
Ek
First
Primero
Pervie
Proto
Aval
Awal
Pahla
Two
Dos
Dva
Dio
Dou
Ethnaim Do
Second
Segundo Vtoroi
Deftero Douvoum
Three
Tres
Tri
Tria
Seh
Third
Tercero
Treti
Trito
Sevoum
Four
Cuatro
Cheterie
Fourth
Cuarto
Five
Maya
Nbu
Nairankiri
Onye-nbu
Phaya
Ibua
Payairi
Onye-ibua
Thalatha Tin
Kimsa
Ito
Thalith
Tisra
Kimsairi
Nke-ito
Tesera Chahaar
Arrbaa
Char
Chetviorti
Tetarto
Rabiek
Chautha Pusiiri
Cinco
Piat
Pente
Khamsa
Panch
Fifth
Quinto
Piati
Pemto Panjoum
Khamis
Panchvan Pheskairi
Nke-ise
Six
Seis
Shest
Exi
Shash
Sitta
Chha
Isi
Sixth
Sexto
Shestoi
Ekto
Shashoom
Sadis
Chhatha Sojjtairi
Chaharoum
Pang
Thani
Dusra
Pusi
Pheschka
Sojjta
Ano
Nke-ano
Ise
Nke-isi

Seven
Siete
Siem
Epta
Haft
Sabaa
Sat
Pakallko
Satvan Pakallkoiri
Isaa
Seventh Septimo Sidmoi
Evthomo Haftoom
Sabieh
Eight
Ocho
Vosiem
Octo
Thamania Ath
Kimsakallko
Asato
Eighth
Octavo
Vosmoi
Ogdoo Hashtoom
Thamin
Athvan
Kimsakallkiri
Nke-asato
Nine
Nueve
Dievit
Enea
Nouh
Tisaa
Nau
Llatunca
Itonu
Ninth
Noveno
Diviati
Enato
Houhum
Tasih
Nauvan Llatuncairi
Mke-Itonu
Ten
Diez
Diesit
Deka
Dah
Ashra
Das
Iri
Tenth
Decimo
Disiati
Dekato Dahoom
Asher
Dasvan Tuncairi
Hasht
Tunca
Nke-isaa
Mke-iri
____________________________________________________________________________________
(1) Ameridian language spoken in Bolivia; (2) Ibo: Eastern Nigeria
Table 5.2. Cardinal and ordinal numbers in different languages
Arithmetical abilities are clearly related with counting. Counting not simply
recording the approximate amount of motor responses required for obtaining reinforcement,
but actually saying aloud a series of number words that correspond to a collection of
objects is relatively recent in human history. Counting also occurs relatively late in child
development. In human history, as well as in child development, counting using number
words begins with sequencing the fingers (i.e., using a correspondence construction) (Hitch
et al., 1987). The name of the finger and the corresponding number can be represented
using the very same word (that means the very same word is used for naming the thumb
and the number one; the very same word is used to name the index finger and the number
two, etc.). The fingers (and toes; as a matter of fact, many languages such as Spanish use
a single word (dedo) to name both the fingers and toes) are usually sequenced in a
particular order. This strategy represents a basic procedure found in different ancient and
contemporary cultures around the world (LevyBruhl, 1910/1947; Cauty, 1984; Klein &
Starkey, 1987; Dansilio, 2008). Interestingly, it has been demonstrated that children with
low arithmetical skills also present a finger misrepresentation on the Draw-a-Person test
(Pontius, 1989). This observation has been confirmed in different cultural groups. By the
same token, difficulty in recognizing and naming the fingers represents a reliable predictor
of developmental dyscalculia (Kaufmann, 2008).
Taking a typical example as an illustration, the Colombian Sikuani or Guahibo
Amazonian jungle Indians (indian-cultures.com/Cultures/guahibo.html) count in the following
way: the person (an adult when counting or a child when learning to count) places his/her
left hand in supination; to point to number one, the right index points to the left little finger,
which is then bent (Queixalos, 1989). The order followed in counting is always from the little
finger to the index. To point to number five, the hand is turned and the fingers opened; for
six, both thumbs are joined, the left fingers are closed, and the right opened; they are
opened one after the other for seven, eight, nine and ten. Between 11 and 20, the head
points to the feet and the sequence is re-initiated. The lexicon used is:
1: kae (the unit, one)
2: aniha-behe (a pair, both)
3: akueyabi
4: penayanatsi (accompanied; that is, the fingers together)
5: kae-kabe (one hand)
Numbers from six to nine, are formed with one hand and (a certain number) of
fingers. Ten becomes two hands:
6: kae-kabe kae-kabesito-nua (one hand and one finger)
7: kae-kabe anih-akabesito-behe (one hand and a pair of fingers)
10: anih-akabe-behe (two hands)

Two hands is maintained between 10 and 20. Toes (taxawusito) are added
between 11 and 14; and one foot (kaetaxu) is used in 15. Twenty is two hands together
with two feet:
11: aniha-kabe-behe kae-taxuwusito (two hands and one toe)
12: aniha-kabe-behe aniha-tuxuwusito-behe (two hands and two toes)
15: aniha-kabe-behe kae-taxu-behe (two hands and one foot)
16: aniha-kae-behe kae-taxu-behe kaetaxuwusito (two hands, one foot, and one toe)
20: aniha-kabe-behe aniha-taxu-behe (two hands and two feet)
Fingers are named according to their order in counting (as mentioned above,
counting begins always with the little finger of the left hand). The Sikuani language
possesses number words only up to three (kae, aniha-behe, akueyabi). Four (penayanatsi
= accompanied, together) represents a correspondence construction. Strictly speaking, the
Sikuani language counts only up to three. From four to twenty, they use a correspondence
construction, not really counting; and for higher quantities, they resort to a global
quantification.
Sometimes not only the fingers (and toes) but also other body segments may be
used in counting: the wrist, the shoulders, the knees, etc. (Levy-Bruhl, 1910/1947; Cauty,
1984; Dansilio, 2008). However, sequencing the fingers (and toes) represents the most
universal procedure in counting. Some languages (e.g., some Mayan dialects and
Greenland Eskimo) use the same word to denote the number 20 (that is, all the fingers
and all the toes) and a person.
In different Amerindian languages, for higher than 10 or 20 figures, most often
many is used (global quantification principle) (Cauty, 1984; Ifrah, 2000). Or, they can refer
to other peoples hands (correspondence construction) (e.g., thirty-five might be something
like my two hands, my two feet, my fathers two hands, my fathers one foot). As
mentioned, twenty sometimes becomes something like one person, a sort of higher
order numeral. It is interesting to note that in some contemporary languages (like English
and Spanish) one means the unit, but it is also used as a sort of indefinite personal
pronoun. In English and Spanish we can also use one as synonymous with myself.
Twenty is found to be the base number in the Mayan numerical system (Swadesh, 1967;
Cauty, 1984). In many contemporary languages, a 10 and/or 20 base is evident.
Digit (from Latin digitus) means both number and finger. The correspondence
construction between numbers and fingers is evident. Latin number notation was originally
Etruscan (Turner, 1984) and referred (as in other languages) to the fingers. One, two, and
three were written simply by making vertical strokes. In four, the Latin system resorts to a
simplification. Originally, four was written IIII, but later on it became IV. Five (V) represented
the whole hand with the arm bent (that is, all the fingers of the hand), and ten (X) the two
arms crossed.
From a neuropsychological perspective, a strong relationship between numerical
knowledge, finger gnosis, and even lateral (rightleft) knowledge is evident (Ardila and
Rosselli, 2002; Kaufmann, 2008). Finger agnosia (and probably rightleft discrimination
disturbances) could be interpreted as a restricted form of autotopagnosia (inability to
recognize or localize the various body parts) (Ardila et al., 1989, 2000).
It is not surprising to find that a decimal (or vigesimal, i.e., with a base of 20) system
has been most often developed. Simultaneously or very close in time, decimal systems
appeared in different countries (Sumer, Egypt, India, and Crete). Different symbols were
used to represent 1, 10, 100, and 1000 (Childe, 1936; Dansilio, 2008) (Figure 5.1.).
Tabla 5.3. Different numerical systems
There is, however, an interesting and intriguing exception: Sumerian and later
Babylonians (about 2,000 BC) developed not only a decimal but also a sexagesimal
system: a symbol represented 60 or any 60-multiple and another different symbol
represented the number 10 and any 10-multiple. Thus, for example, the number 173 was
then represented: 2 60 (the symbol for 60 repeated twice) + 5 10 (the symbol for 10
repeated five times) + 3 (a symbol for units repeated three times). A base of 60 has
remained for some contemporary time measures (e.g., minutes and seconds). Twelve is
also frequently maintained as a second-order unit (e.g., a dozen). Evidently, 60 results
from five times twelve. Five obviously is one hand, and the question becomes, where
does 12 come from? What are the two additional units? It might be speculated that 12
means the 10 fingers plus the two feet or even the two elbows or the two shoulders or the
two knees (individuality of components is easier to appreciate in the hands than in the feet).
But this is only speculation, although it is feasible according to our knowledge about
counting procedures used in different cultural groups (Levy-Bruhl, 1910/1947; Ifrah, 2000;
Dansilio, 2008).
Maya Indians developed a similar system, but had 20 as a base (Leon-Portilla,
1986). They used different symbols to represent 20, 400 (20 20), and 8000 (20 20 20)
(Cauty, 1984) (Figure 5.1.)
Figure 5.1. Maya vigesimal numerical system.
Thus, reviewing the history of numerical concepts, it is found that world languages
developed a base 10 (10 fingers) or 20 (10 fingers plus 10 toes) or even five (five fingers)
to group quantities. In some contemporary languages a residual 20-base can be found
(e.g., in French 80 can be four twenties). In many contemporary languages, different
words are used between 1 and 10. Between 10 and 20, the numerical systems usually
become irregular, unpredictable, and idiosyncratic. From 20 onward, numbers are formed
simply with the words twenty plus one, twenty plus two, etc. Some contemporary
languages still use a five-base in counting. For instance, in the Amerindian language
Tanimuca in South America (www.ethnologue.com), speakers count up to five. Between
five and 10, numbers are five one, five two, and so on.
Further developments of arithmetical abilities

Writing numbers appeared earlier in history than writing language. Some cultures (e.g.,
Incas) developed a number representing system, but not a language representing system
(Swadesh, 1967). As mentioned before, calculus means pebble. Pebbles, marks, knots,
or any other element were used as a correspondence construction to record the number of
elements (people, cows, fishes, houses, etc). In Sumer, the first number writing system has
been found (about 3,000 BC) (Childe, 1936; Ifrah, 2000): Instead of using pebbles, fingers,
or knots, it was simpler just to make a mark (a stroke or a point) on the floor, on a tree
branch, or on a board if one wanted to keep the record. In Egypt, India and later in Crete, a
similar system was developed: units were represented by a conventional symbol (usually a
stroke) repeated several times to mean a digit between one and nine; a different symbol
was used for 10 and 10-multiples. Incas Indians developed a special system to represent
numbers with knots in a rope (quipus) (Ascher & Ascher, 1980) (Figure 5.2).
Positional digit value is clearly evident in Babylonians, and around 1,000 BC, the zero was
introduced. Positional value and zero are also evident in Maya Indians (Leon-Portilla,
1986). Egyptians and Babylonians commonly used fractions. Small fractions (1/2, 1/3, and
1/4) are relatively simple numerical concepts, and even chimpanzees can be trained to use
small fractions (Woodruff & Premack, 1981).
As pointed out, recognition of individual marks or elements up to three is easy: It
represents an immediate perception readily recognizable. Beyond three, the number of
marks (strokes or dots) usually has to be counted and errors are more likely. Furthermore,
it is rather time-consuming and cumbersome to be constantly counting marks. Interestingly,
the different digit notational systems always represent one, two and three with strokes (or
points, or any specific mark). In other words, the numbers one, two and three are written
making one, two or three strokes. But beyond these figures, digit writing may give way to
other strategies. In our Arabic digit notation system, one is a vertical line whereas two and
three were originally horizontal lines that became tied together by being handwritten (Ifrah,
2000). This observation may be related with the inborn ability to perceptually recognize up
to three elements. Beyond three, errors become progressively more likely. Perceptually distinguishing eight and nine strokes is not as easy as distinguishing between two and three
strokes. The introduction of a different representation for quantities over three was a useful
and practical simplification.
Figure 5.2. Example of an Inca Indian quipu.
The numerical system, along with measurement units, were developed departing
from the body dimensions (fingers, hands, arm, steps, etc.). This tendency to use the
human body not only to count but also as measure units is still observed in some contemporary measurement units (e.g., foot).
Adding, subtracting, multiplying and dividing were possible in the Egyptian system,
but of course, following procedures was quite different from those procedures we currently
use. Egyptians based multiplication and division on the duplication and halving method
(Childe, 1936). Interestingly, this very same procedure (duplicating and halving quantities)
is also observed in illiterate people when performing arithmetical operations. Thus, to
multiply 12 18 in the Egyptian system the following procedure was followed:
18
36
*4
72
*8
144
_____
Total
216
(The number 18 is duplicated one or several times, and the amounts corresponding to 12
(4 + 8 in this example) are selected and summed up: 72 + 144 = 216. To divide, the inverse
procedure was used. Therefore, the procedure used to divide 19 by 8 would be:
1
*2
16
*4
*8
That is, 2 + 4 + 8 (2 + 1/4 + 1/8), which is 2.375

In brief, different steps were followed in the development of arithmetical abilities:
representing quantities, initially as correspondence constructions (i.e., one mark represents
one element), later new marks were added to represent larger quantities (usually 10);
providing a positional value to the marks; using fractions; and computing quantities (adding
and subtracting; and later multiplying and dividing). As pointed out, recognition of individual
marks or elements up to three is easy: It represents an immediate perception readily
recognizable. Beyond three, the number of marks (strokes or dots) usually has to be
counted and errors are more likely. Furthermore, it is rather time-consuming and
cumbersome to be constantly counting marks. Interestingly, the different digit notational
systems always represent one, two and three with strokes (or points, or any specific mark).
In other words, the numbers one, two and three are written making one, two or three
strokes. But beyond these figures, digit writing may give way to other strategies. In our
Arabic digit notation system, one is a vertical line whereas two and three were originally
horizontal lines that became tied together by being handwritten (Ifrah, 2000) (Figure 5.3.)
This observation may be related with the inborn ability to perceptually recognize up to three
elements. Beyond three, errors become progressively more likely. Perceptually distinguishing eight and nine strokes is not as easy as distinguishing between two and three
strokes. The introduction of a different representation for quantities over three was a useful
and practical simplification.
Figure 5.3. Origins of the Arabic numbers 1, 2 and 3.
The numerical system, along with measurement units, was developed departing
from the body dimensions (fingers, hands, arm, steps, etc.). This tendency to use the
human body not only to count but also as measure units is still observed in some contemporary measurement units (e.g., foot).
The neuroscience of calculation abilities

Since primary acalculia (a basic defect in computational ability) was initially described by
Henschen (1925) it has been associated with left posterior parietal damage (e.g., Mazzoni
et al., 1990; Ardila et al., 2000; Mayer et al., 2003). Furthermore, it was suggested that
different cerebral pathways are responsible for processing rote numerical knowledge (e.g.,
multiplication tables) and semantic knowledge of numerical quantities. Dehaene and Cohen
(1997) have proposed that a left subcortical network contributes to the storage and retrieval
of rote verbal arithmetical facts, whereas an inferior parietal network is dedicated to the
mental manipulation of numerical quantities.
Neuroimaging techniques (e.g., fMRI) have been used to analyze the pattern of
brain activity during diverse calculation tasks. It has been demonstrated that different brain
areas are active during arithmetical tasks, but the specific pattern of brain activity depends
on the particular type of task that is used. At minimum, the following brain areas become
activated during calculation: the upper cortical surface and anterior aspect of the left middle
frontal gyrus (Burbaud et al., 1995); the supramarginal and angular gyrus (bilaterally)
(Rueckert et al., 1996); the left dorsolateral prefrontal and premotor cortices, Brocas area,
and the inferior parietal cortex (Burbaud et al., 1999); and the left parietal and inferior
occipitotemporal regions (lingual and fusiform gyri) (Rickard et al., 2000). The diversity of
brain areas involved in arithmetical processes supports the assumption that calculation
ability represents a multifactor skill, including verbal, spatial, memory, body knowledge, and
executive function abilities (Ardila & Rosselli, 2002). Dehaene et al. (2004), however,
proposed that regardless of the diversity of areas that become active during arithmetical
tasks, the human ability for arithmetic is associated with activation of very specific brain
areas, in particular, the intraparietal sulcus (Figure 5.4). Neuroimaging studies with humans
have demonstrated that the intraparietal sulcus is systematically activated during a diversity
of number tasks and could be regarded as the most crucial brain region in the
understanding and use of quantities (Ashkenazi et al., 2008). These observations have
been supported using brain electrostimulation (Roux et al., 2009). Other brain areas, such
as the precentral area, the inferior prefrontal cortex, and the inferior parietal cortex are also
activated when subjects engage in mental calculations (Kas et al., 2011). Roca (2009)
has proposed that there exists a frontoparietosubcortical circuit responsible for complex
arithmetic calculations and that procedural knowledge relies on a visuo-spatial sketchpad
that contains a representation of each sub-step of the procedure.
Figure 5.4. Left hemisphere intraparietal sulcus.
Traditionally, calculation defects have been associated with posterior left parietal
damage (Henschen, 1925; Boller & Grafman, 1983), and are frequently included in the socalled Gerstmanns (or angular gyrus) syndrome. Symptoms of Gerstmanns syndrome
(acalculia with agraphia, disorders in right-left orientation, and finger agnosia) (Gerstmann,
1940) can be found during direct cortical stimulation in the angular gyrus region (Roux et
al., 2003). Using fMRI, it has been observed that the left angular gyrus is not only involved
in arithmetic tasks requiring simple fact retrieval, but may show significant activations as a
result of relatively short training of complex calculation (Delazer et al., 2003).
Colvin et al. (2005) investigated numerical abilities in a split-brain patient using
experiments that examined the hemispheres abilities to make magnitude comparisons.
One experiment examined the ability to enumerate sets of stimuli, and another two
experiments required judgments about two concurrently presented stimuli that were either
identically coded (i.e., two Arabic numerals, two number words, or two arrays of dots) or
differently coded (e.g., an Arabic numeral and a number word). Both hemispheres were
equally able to enumerate stimuli and make comparisons between numerical
representations regardless of stimuli coding. However, the left hemisphere was more
accurate than the right when the task involved number words.
Cohen et al. (2000) reported a patient with a lesion in the left perisylvian area who
showed a severe impairment in all tasks involving numbers in a verbal format, such as
reading aloud, writing to dictation, or responding verbally to questions of numerical
knowledge. In contrast, her ability to manipulate non-verbal representation of numbers, i.e.,
Arabic numerals, was comparatively well preserved. This observation supports the proposal
that language and calculation disorders can be dissociated (Basso et al., 2000). Some
authors have assumed that language and numerical concepts are organized differently in
the brain and follow distinct developmental patterns in children (Gelman & Butterworth,
2005). Other authors have suggested that calculation and language are mediated by
partially different and also partially overlapped brain systems (Baldo & Dronkers, 2007).
Semenza et al. (2006) have emphasized that calculation and language usually share the
same hemisphere.
In summary, diverse brain areas are activated during the performance of different
arithmetical tasks, although contemporary evidence suggests that the intraparietal sulcus
seems to play the most crucial role. During the learning of new calculation abilities,
additional brain areas become involved and the specific pattern of brain activity depends on
the particular type of test that is used. It can be assumed that during human history, the
development of new numerical abilities was correlated with the involvement of new brain
areas during the performance of progressively more complex numerical tasks.
Conclusion
Arithmetical abilities and number representation have existed for only some 50006000
years. Most likely, during the Stone-Age, only simple counting up to three and, of course,
bigger and smaller (magnitude judgment) concepts were present. Global quantification is
observed at the pre-human level. Correspondence constructions allowed for increasing the
amount of numbers to be used. The most immediate correspondence construction is
performed with the fingers. Finger knowledge and counting represent, to a certain extent,
the same cognitive ability, as is still evident in some contemporary languages, such as
Sikuani.
Counting, finger gnosis, and even lateral spatial knowledge may present a common
historical origin. Seemingly, calculation abilities were derived from finger sequencing.
Number representation and arithmetical operations are observed only since some 5000
6000 years ago. Currently, calculation abilities are rapidly evolving due to the introduction
of modern technology and resulting cognitive demands. Right-left discrimination (as well as
the use of other spatial concepts) most likely was present in pre-historic man, because
requirements of spatial abilities may have been very high, even higher than in
contemporary man (Hours, 1982; Ardila and Ostrosky, 1984; Ardila, 1993). Right-left
discrimination and finger gnosis are strongly interdependent, and they can even be interpreted as components of the autotopagnosia syndrome. It seems, in consequence, that
there is a rationale for finding a common brain activity for finger gnosis, calculation, and
right-left discrimination (and in general, spatial knowledge mediated by language) (Ardila
and Rosselli, 2002).
Contemporary neuroimaging techniques, specifically fMRI, have demonstrated that
the left parietal lobe, particularly the intraparietal sulcus, is systematically activated during a
diversity of number tasks; other areas, particularly the frontal lobe, are also involved in
processing numerical information and solving arithmetical problems. Also, it has been
suggested there exists a frontoparietosubcortical circuit responsible for complex
arithmetic calculations and procedural knowledge.
It can be conjectured that numerical abilities continue evolving due to advances in
mathematical knowledge and the introduction of new technologies; for instance, instead of
writing numbers down on paper and applying certain computational rules, we more often
require the ability to use a pocket calculator or a computer program. Doubtless,
computation ability is evolving in a new direction. Brain representation of calculation may be
taking a new direction, and even the acalculia syndrome may present different clinical
manifestations.
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6. Origins of Executive Functions3
Introduction
"Executive functions" is a relatively new term in the neurosciences. Luria (1966, 1973,
1980) is the direct antecessor of the concept of executive functions. He distinguished three
functional units in the brain: (1) arousal-motivation (limbic and reticular systems); (2)
receiving, processing, and storing information (post-rolandic cortical areas); and (3)
programming, controlling, and verifying activity, depending on the activity of the prefrontal
cortex (Figure 6.1). Luria mentions that this third unit has an executive role. Lezak (1983)
referred to "executive functioning" to discriminate cognitive functions from the "how" or
"whether" of human behaviors. Baddeley (1986) grouped these behaviors into cognitive
domains that included problems in planning, organizing behaviors, disinhibition,
perseveration, reduced fluency, and initiation. Baddeley also coined the term "dysexecutive
syndrome."
3 A previous version of this paper was published in: Ardila, A. (2008). On the evolutionary origins of executive
functions. Brain and Cognition, 68, 92-99
Figure 6.1. Three functional units in the brain (Luria, 1966, 1973, 1980)
What does executive functions mean?

The definition of executive function includes the concept of mental flexibility and also
ability to filter, interference, engage in goal-directed behaviors, and anticipate the
consequences of one's actions (Ardila & Surloff, 2007; Denckla, 1994, 1996; Goldberg,
2001; Luria 1969, 1980; Stuss & Benson 1986; Stuss & Knight, 2002). The concept of
morality, ethical behaviors, self-awareness, and the idea of the frontal lobes as manager
and programmer of the human psyche are also included (Anderson et al., 1999; Damasio,
1994; Moll et al., 2005; Luria, 1980).
During the late 19th and early 20th centuries, clinical investigations documented
diverse behavioral disorders in cases of frontal pathology. "Frontal lobe syndrome" was
conceptualized by Feuchtwanger (1923). He correlated frontal pathology to behaviors that

were not related to overt speech, memory, or sensorimotor deficits. He emphasized the
personality changes in motivation, affective dysregulation, and the capacity to regulate
and integrate other behaviors. Goldstein (1944) expanded the capacity of frontal lobe
behaviors to include "the abstract attitude," initiation, and mental flexibility. Luria (1966,
1969) related prefrontal lobe activity with programming motor behavior, inhibiting
immediate responses, abstracting, problem solving, verbal regulation of behavior, and
reorienting behavior according to behavioral consequences, temporal integration of
behavior, personality integrity, and consciousness. During the 1970s, 1980s, and 1990s
several books exclusively devoted to the analysis of the prefrontal cortex were published
(e.g., Fuster, 1989; Miller & Cummings, 1998; Levin et al., 1991; Perecman, 1987;
Pribram & Luria, 1973; Roberts, 1998; Stuss & Benson, 1986). These works usually
assumed that "frontal" ("prefrontal") syndrome was synonymous with executive
dysfunction (Figure 6.2).
Progressively, it became apparent that prefrontal syndrome and executive
dysfunction are not synonymous. The prefrontal cortex plays a key monitoring role in
executive functions, but other brain areas are also involved (Elliott, 2003). Intact frontal
processes, although not synonymous with intact executive functioning, are an integral part
of it. Attempts to localize executive functioning to discrete frontal areas have been
inconclusive. The emerging view is that executive function is mediated by dynamic and
flexible networks. Neuroimaging results have also implicated posterior, cortical, and
subcortical regions in executive functioning (Park et al., 2011; Roberts et al., 2002).
Figure 6.2. Frontal lobe and its major areas.
Historically, Phineas Gage has become the most classical example for prefrontal
lobe pathology and disturbances in executive functions (Harlow 1868) (Figure 6.3).
Phineas Gage was a reliable foreman for a railroad company who suffered a tragic
accident in which a tampering rod was projected through his frontal lobes. Miraculously he
survived, but after this accident, he was described as "profane," "irascible," and
"irresponsible." Profound personality changes were reported, and according to Harlow, he
began to behave as an animal. The Phineas Gage case is usually cited as a typical
example of executive function disturbances. It is obvious however, that Phineas Gages
impairments were mostly situated at an emotional/motivational level, not at a purely
cognitive (or metacognitive) level. Overt behavioral changes were observed as
frequently found in frontal lobe pathology, but purely cognitive impairments were illdocumented, partially due to the lack of appropriate cognitive assessment instruments.
Most frequently, executive functions are analyzed in experimental conditions using
diverse research strategies, such as solving diverse problems, finding similarities between
two words, providing an answer that requires inhibiting another, etc. A paradigm is
created, and the subject is required to solve it. The brain activity can be simultaneously
recorded, using brain electrical activity or recording the regional level of activation (e.g.,
Osaka, 2004). Alternatively, executive functions are analyzed in brain-damaged
populations in order to find the contribution of different brain systems (e.g., Jacobs et al.,
2007). This last approach represents the classical neuropsychological method. Executive
functions, however, rarely are analyzed in natural ecological conditions. How is it that
people solve everyday problems? This is obviously a crucial question in understanding
human behavior.
Figure 6.3. Reconstruction of the wound suffered by Phineas Gage (according to

Damasio et al., 1994)
Tests for executive function typically represent external tasks, requiring the correct
application of some intellectual abilities to be solved; for example, the Wisconsin Card
Sorting Test (Berg, 1948; Heaton, 1981), the Tower of Hanoi (Simon, 1975) (Figure 6.4),
and the Stroop test (Stroop, 1935) represent unusual and unfamiliar tasks, requiring the
development of new strategies, planning, thought, flexibility, etc. Nonetheless, they are
emotionally neutral tasks.
Figure 6.4. Tower of Honoi as an example of an executive functions test.
Although executive functions depend on extended networks including different

brain areas, it is assumed that the prefrontal cortex plays a major controlling and
monitoring role. Most important, prefrontal cortex does not only participate in those
classically recognized executive operations (sequencing, alternating, inhibiting, etc), but
also plays a crucial role in coordinating cognition and emotion (Mitchell & Phillips, 2007).
Most of the disturbances reported in Phineas Gage (and in many other cases of prefrontal
syndromes) refer to behavioral/emotional disturbances; or more exactly, disturbances in
coordinating cognition and emotion/motivation. The prefrontal lobe has extensive
connections to the subcortical and limbic system areas (Barbas, 2006; Damasio &
Andersen, 1993) and even its orbital portion could be regarded as an extension of the
limbic system. It seems that no laboratory test for executive function taps into the ability to
coordinate cognition and emotion, and in that regard, no executive function test has
significant ecological validity.
By coordinating cognition and emotion, the prefrontal lobe plays a major function:
controlling the limbic system impulses; that is, making limbic impulses socially
acceptable (e.g., Beer, John, Scabini & Knight, 2006; Blair, 2004; Lezak et al., 2004).
The inability to make basic biological needs socially acceptable, as clearly described in
Phineas Gages case, frequently represents a major disturbance in prefrontal patients. Of
course, we all would like to hit somebody when frustrated, to take possession of anything
we want, to stay at home instead of performing fatiguing work, and to approach any
potential sexual partner. That is exactly what many patients with prefrontal lobe pathology
frequently do.
Is there any fundamental core ability accounting for executive

functions?
Some disagreement exists around the question of unity or diversity (non-unitary) of
executive functions (e.g., Duncan et al., 1996; de Frias, Dixon & Strauss, 2006; Grafman,
2006; Kimberg, dEsposito & Farah, 1997; Parkin & Java, 1999; Stuss, 2011). It is not clear
what the particular unitary factor saturating the different executive function tests is.
Behavior inhibition has been considered as a potential candidate for the single factor
responsible for successful performance in different executive tests (Barkley, 1997) or in
combination with working memory (Pennington & Ozonoff, 1996). Salthouse (1996, 2005)
suggested that reasoning and perceptual speed represent the underlying factors related to
all executive functions. Salthouse (2005) observed that performance on two common tests
of executive functioning, the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981) and
the Controlled Oral Word Association Test (Benton, Hamsher & Sivan, 1994), were strongly
correlated with reasoning ability and perceptual speed.
Other authors challenge the existence of such a unitary factor. Godefroy et al.
(1999) emphasized that certain frontal lobe patients perform well on some tests purported
to assess executive abilities but not on others. Correlations among different executive tests
are frequently moderate or low, and many times lacking statistical significance (Lehto,
1996; Friedman et al., 2006; Salthouse, Atkinson & Berish, 2003).
Miyake et al. (2000) adopted an intermediate position. They studied three oftenpostulated aspects of executive functions (shifting, updating, and inhibition) and concluded
that, although they are clearly distinguishable, they do share some underlying commonality.
Based on the results of their study, the authors stated that executive functions are
separable but moderately correlated constructs thus suggesting both unitary and nonunitary components of the executive system. By the same token, several authors have
suggested different subcomponents of executive functions (e.g., Anderson, 2001; Delis,
Kaplan & Kramer, 2001; Denckla 1994; Elliot, 2003; Hobson & Leeds, 2001; Lafleche &
Albert, 1995; Lezak, 1983; Piguet et al., 2002).
Stuss (2011) states that specific frontal regions control discrete functions and those
very basic cognitive processes can be systematically manipulated to reveal those functions.
According to him, recent studies have demonstrated consistent anatomical/functional
relationships: dorsomedial for energization, left dorsolateral for task setting, and right
dorsolateral for monitoring, and consequently, there is no central executive. There are,
instead, numerous domain general processes discretely distributed across several frontal
regions that act in concert to accomplish control. Stuss further supports the point of view
that there are two additional "frontal" anatomical/functional relationships: ventral-
medial/orbital for emotional and behavioral regulation, and frontopolar for integrative-even
meta-cognitive-functions.
Two proposed fundamental executive functions

It may be conjectured that there are two different, but closely related types, of prefrontal
lobe abilities (e.g., Fuster, 2002; Happaney, Zelazo, & Stuss, 2004; Stuss, 2011):
(1) Metacognitive executive functions which include problem solving,
abstracting, planning, strategy development and implementation, and working memory
(the usual understanding of executive functions, generally measured in neuropsychology
executive functions tests); these are abilities mostly related with the dorsolateral area of
the prefrontal cortex (e.g., Stuss & Knight, 2002).The dorsolateral prefrontal cortex has
been observed to participate in diverse planning, abstracting, problem solving, and
working memory tasks. Using fMRI dorsolateral prefrontal activation has been found in
tasks such as solving the Tower of Hanoi (Fincham, Carter, van Veen, Stenger &
Anderson, 2002), Controlled Word Association Test (letter fluency) (Baldo, Schwartz,
Wilkins & Dronkers, 2006), working memory (Yoon, Hoffman & D'Esposito, 2007), and
solving the Wisconsin Card Sorting Test (Lie, Specht, Marshall & Fink, 2006).
(2) Emotional/motivational executive functions, which is responsible for
coordinating cognition and emotion. That means, the ability to fulfill basic impulses
following socially acceptable strategies. In the last case, what is most important does not
necessarily include what the best conceptual and intellectual result is, but what is in
accordance with personal impulses (e.g., Bechara, Damasio & Damasio, 2000). In that
regard, the core function of the prefrontal lobe is to find acceptable justifications for limbic
impulses. Following socially acceptable strategies actually involves inhibition of selfish or
unsociable basic impulses in the first place, but not necessarily arriving at the best
conceptual solution. The ventromedial areas of the prefrontal cortex are involved in the
expression and control of emotional and instinctual behaviors (Fuster, 1997, 2002). This
function is related with so-called inhibitory control of behavior (Miller & Wang, 2006).
Clinical evidence (e.g., Luria, 1969; Stuss & Knight, 2002) as well as experimental
research (e.g., Leung & Cai, 2007; Medalla, Lera, Feinberg & Barbas, 2007) suggest that
the neural substrate for this inhibitory function resides mainly in the medial and orbital
portions of the prefrontal cortex.
Fuster ( 2002) points out that The apparent
physiological objective of inhibitory influences from orbitomedial cortex is the suppression

of internal and external inputs that can interfere with whatever structure of behavior,
speech, or cognition is about to be undertaken or currently underway (page 382).
There is no question that if metacognitive executive functions were indeed used in
solving external problems without the involvement of limbic impulses, most world-wide
problems would have been solved by man, because contemporary man has sufficient
resources to solve all the major social problems (such as poverty and war). Human
conflicts in general would also be significantly reduced.
Direct observation suggests that everyday problems usually have an emotional
content: talking with a friend, a boss or a spouse; driving in the street; deciding how to
approach somebody; spending money, etc., are not emotionally neutral activities, as are
the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981) and the Tower of Hanoi
(Simon, 1975). When other people are involved, it is not easy to remain emotionally
neutral. Social issues, simply speaking, are not emotionally neutral, because
power/submission, personal benefits, and diverse biological drives are potentially involved
(Smith, Bond & Kagitcibas, 2006). Most likely, throughout evolution of mankind (i.e.,
during the last 150,000 years) fulfilling these drives has been the major application of the
prefrontal functions: to get power, to have a dominant role, to take food and goods for
ourselves, to get a sexual partner, etc. That means that emotional/motivational executive
functions have played a crucial role in survival and reproduction (e.g., facilitating
behaviors such as acquiring dominant roles, obtaining sexual partners, etc).
Mitchell and Phillips (2007) have argued that emotion can affect executive function
ability. They propose that mild manipulations of negative mood appear to have little effect
on cognitive control processes, whereas positive mood impairs aspects of updating,
planning and switching. This effect of emotion on cognition has been supported for
different executive function tasks, such as working memory (Spies, Hesse & Hummitzsch,
1996) and planning (Oaksford, Morris, Grainger & Williams, 1996) and using the Tower of
London (Shallice, 1982) as a paradigm. In other words, when emotion is involved,
metacognitive executive function ability decreases. Mitchell and Phillips (2007) emphasize
that current evidence on the effects of mood on regional brain activity during executive
functions demonstrates that the prefrontal cortex represents an area of integration
between mood and cognition.
These two types of executive functions (metacognitive and emotional/
motivational) depend on relatively different prefrontal areas, and as a matter of fact, two
major variants in the prefrontal syndrome are frequently distinguished: one mostly
impairing cognition (or rather, cognitive control, that is, metacognition); the other one
mostly impairing behavior:
(1) Dorsolateral syndrome. Cummings (1993) indicated that the dorsolateral
circuit is the most important to executive functioning (Figure 6.5). The most noted deficit is
an inability to organize a behavioral response to novel or complex stimuli. Symptoms are
on a continuum and reflect capacity to shift cognitive sets, engage existing strategies, and
organize information to meet changing environmental demands. Various researchers,
including Luria (1969), have noted perseveration, stimulus-bound behavior, echopraxia,
and echolalia. Lateralization has been noted in executive dysfunction (Goldberg, 2001).
Ventral and dorsal portions of prefrontal cortex are bilieved to interact in the maintenance
of rational and nonrisky decision making (Manes et al., 2002). According to Fuster
(1997, 2002), the most general executive function of the lateral prefrontal cortex is the
temporal organization of goal-directed actions in the domains of behavior, cognition, and
language.
Figure 6.5. Location of the dorsolateral prefrontal cortex.
(2) Orbitofrontal and medial frontal syndrome. Orbitofrontal damage has been
associated with desinhibition, inappropriate behaviors, personality changes, irritability,
mood liability, tactlessness, distractibility, and disregard of important events (Stuss &
Knight, 2002). These patients are unable to respond to social cues. Noteworthy, it was
observed by Laiacona and colleagues (1989) that these patients have no difficulty with
card-sorting tasks. Eslinger and Damasio (1985) coined the term "acquired sociopathy" to
describe dysregulation that couples both a lack of insight and remorse regarding these
behaviors. The orbitofrontal cortex appears to be linked predominantly with limbic and
basal forebrain sites. Medial frontal lobe damage causes apathy or abulia (a severe form
of apathy). Acute bilateral lesions in the medial frontal area can cause akinetic mutism, in
which the individual is awake and has self awareness, but does not initiate behaviors
(Ross & Stewart, 1981). According to Fuster (1997, 2002) the ventromedial areas of the
prefrontal cortex are involved in expression and control of emotional and instinctual
behaviors (Figure 6.6).
It is evident that the two prefrontal syndromes can have rather different clinical
expressions (metacognitive and emotional/motivational) depending upon the specific

location of the damage.
Figure 6.6. Location of the orbitofrontal cortex.
Metacognitive executive functions as an internalization of actions

As pointed above, disagreement persists around the potential unitary factor in executive
functions. I will suggest that action representation (i.e., internally representing
movements) may constitute at least one basic metacognitive executive function factor. I
will refer to action representation and time perception, derived from it; both ultimately
potentially depending upon one single core ability (sequencing?).
Two departing observations are important to support the involvement of the
prefrontal cortex in motor representation:
1. Anatomical observation: Prefrontal cortex represents an extension and further

evolution of the frontal motor areas. It may be conjectured that the prefrontal lobe should
participate in complex and elaborated motor (executive) activities.
2. Clinical observation: A diversity of motor control disturbances are observed in
prefrontal pathology, such as perseveration, utilization behavior, paratonia, primitive
reflexes, etc. (e.g., Ardila & Rosselli, 2007a; Victor & Ropper, 2001).
Several authors have argued that thought, reasoning, and other forms of complex
cognition (metacognition) depend on an interiorization of actions. Vygotsky (1929,
1934/1962, 1934/1978), for instance, proposed that thought (and in general, complex
cognitive processes) is associated with some inner speech. Vygotsky represents the most
classical author suggesting this interpretation for complex cognition. More recently,
Lieberman (2002a, 2002b) suggested that language in particular and cognition in general
arise from complex sequences of motor activities.
Vygotsky (1934/1978) developed the concept of extracortical organization of
higher mental functions to account for the interaction of biological and cultural factors in
the development of human cognition. Vygotskys (1934/1962, 1934/1978) understanding of
higher mental functions is roughly equivalent to metacognitive executive functions.
According to Vygotsky, a major factor in systemic organization of higher cognitive
processes is the engagement of external instruments (objects, symbols, signs), which have
an independent history of development within culture. Vygotsky called this principle of
construction of brain functional systems the principle of extracortical organization of
complex mental functions, implying that all types of mankinds conscious activities are
formed with the support of external auxiliary tools or aids. However, different mediators and
means, or significantly different details within them, (e.g., the direction of writing and degree
of letter-sound correspondence, orientation by maps or by the behavior of sea-birds, etc.,)
may develop, and in fact are developed in different cultures. Therefore, the analysis of
cognitive processes must necessarily take into account these cross-cultural differences
(Kotik-Friedgut & Ardila, 2004).
The central point in Vygotskys (1934/1962) idea is that higher forms of cognition
(cognitive executive functions) depend on certain mediation (language, writing or any
other); the instruments used for mediating these complex cognitive processes are culturally
developed. According to Vygotsky (1934/1962), the invention (or discovery) of these
instruments will result in a new type of evolution (cultural evolution), not requiring any
further biological changes. Thinking is interpreted as a covert motor activity (inner
speech).
Vygotsky (1929) assumes that thought and speech develop differently and
independently having different genetic roots. Before two years of age, the development of
thought and speech are separate. They converge and join at about the age of two years,
and thought from this point on becomes language mediated (verbal thought). Language in
consequence becomes the primary instrument for conceptualization and thinking.
According
to
Vygotsky
(1934/1962),
speech
develops
first
with
external
communicative/social speech, then egocentric speech, and finally inner speech.

Vocalization becomes unnecessary because the child "thinks" the words instead of
pronouncing them. Inner speech is for oneself, while external, social speech is for others.
Vygotsky considered that thought development is determined by language.
Vygotsky (1987) separated two different types of concepts: spontaneous and
scientific. Spontaneous concepts are developed in a parallel way with language, whereas
scientific concepts are concepts learned at school. Children progressively develop reflective
consciousness through the development of scientific concepts. School is intimately related
with learning a new conceptual instrument: reading. Written language is an extension of
oral language, and represents the most elaborated form of language.
Luria further extended Vygotskys ideas and attempted to find the neurological
correlates for different components of complex cognitive processes. He clearly stated that
mental functions are social in origin and complex and hierarchical in their structure and
they all are based on a complex system of methods and means... (Luria, 1973; p. 30).
In brief, Vygotsky (1934/1962) argued that complex psychological processes

(metacognitive executive functions) derives from language internalization. Thinking relies
on the development of an instrument (language or any other) that represents a cultural
product.
Lieberman (2002a, 2002b) refers specifically to the origins of language. He
postulates that neural circuits linking activity in anatomically segregated populations of
neurons in subcortical structures and the neocortex throughout the human brain regulate
complex behaviors such as walking, talking, and comprehending the meaning of sentences.
The neural substrate that regulates motor control (basal ganglia, cerebellum, frontal cortex)
in the common ancestor of apes and humans most likely was modified to enhance cognitive
and linguistic ability. Lieberman (2002a, 2002b) suggests that motor activity is the departing
point for cognition. Speech communication played a central role in this process. The neural
bases of mankinds linguistic abilities are complex, involving structures other than Brocas
and Wernickes areas. Many other cortical areas and subcortical structures form part of the
neural circuits implicated in the lexicon, speech production and perception, and syntax. The
subcortical basal ganglia support the cortical-striatal-cortical circuits that regulate speech
production, complex syntax, and the acquisition of the motor and cognitive pattern
generators that underlie speech production and syntax. They most likely are involved in
learning the semantic referents and sound patterns that are instantiated as words in the
brains dictionary.
The cerebellum and prefrontal cortex are also involved in learning motor acts (e.g.,
Hernandez-Mueller et al., 2005; Matsumura et al., 2004). Lieberman (2002a, 2002b)
proposes that the frontal regions of the cortex are implicated in virtually all cognitive acts
and the acquisition of cognitive criteria; posterior cortical regions are clearly active elements
of the brains dictionary. The anterior cingulate cortex plays a part in virtually all aspects of
language and speech. Real-word knowledge appears to reflect stored conceptual
knowledge in regions of the brain traditionally associated with visual perception and motor
control. Some aspects of human linguistic ability, such as the basic conceptual structure of
words and simple syntax, are phylogenetically primitive and most likely were present in the
earliest hominids. Lieberman (2002a, 2002b) further suggests that speech production,
complex syntax, and a large vocabulary developed in the course of hominid evolution, and
Homo erectus most likely talked, had large vocabularies, and commanded fairly complex
syntax. Full human speech capability, enhancing the robustness of vocal communication,
most likely is a characteristic of anatomically modern humans.
These two authors (Vygotsky and Lieberman), although using rather different
approaches, have both postulated that the development of language and complex cognition
are related with some motor programs, sequencing, internalizing actions, and the like.
The recent discovery of so-called mirror neurons represents a new element in
understanding inner speech and action representation. A mirror neuron is a neuron which
fires both when an animal performs an action and also when the animal observes the same
action performed by another animal. In humans, brain activity consistent with mirror
neurons has been found in the premotor cortex and the inferior parietal cortex (Rizzolatti et
al., 1996; Rizzolatti & Craighero, 2004). In monkeys, the rostral part of ventral premotor
cortex (area F5) contains neurons that discharge, both when the monkey grasps or
manipulates objects and when it observes the experimenter performing similar actions.
These neurons (mirror neurons) appear to represent a system that matches observed
events to similar, internally generated actions.
Transcranial magnetic stimulation and positron emission tomography (PET)
experiments suggest that a mirror system for gesture recognition also exists in humans and
includes Broca's area (Rizzolati & Arbib, 1998). The discovery of mirror neurons in the
Brocas area might have immense consequences for understanding the organization and
evolution of mankind cognition (Arbib, 2006; Craighero, Metta, Sandini & Fadiga, 2007). An
obvious implication of mirror neurons is that they can participate in the internal
representation of actions. Neuroimaging data have showed that interactions involving
Broca's area and other cortical areas are weakest when listening to spoken language
accompanied by meaningful speech-associated gestures (hence, reducing semantic
ambiguity), and strongest when spoken language is accompanied by self-grooming hand
movements or by no hand movements at all suggesting that Brocas area may be involved
in action recognition (Skipper, Goldin-Meadow, Nusbaum & Small, 2007). PET studies have
associated the neural correlates of inner speech with activity of the Brocas area (McGuire,
Silbersweig, Murray, David, Frackowiak & Frith, 1996).
Is there anything special in the prefrontal cortex?

For some time it has been assumed that the prefrontal cortex is significantly larger in
humans than in other primates (e.g., Blinkov & Glezer, 1968). This difference in volume
was assumed to represent a major reason to account for differences in complex forms of
cognition (executive functions) observed in humans.
Nonetheless, such an assumption turned out to be incorrect. Measures of prefrontal
lobe volumes have not found differences between mankind and non-human primates.
Semendeferi et al (1997, 2002) measured the volume of the frontal lobe as a whole and of
its main sectors (including cortex and immediately underlying white matter) in humans,
chimpanzees, gorillas, orangutans, gibbons, and macaques using three-dimensional
reconstructions of magnetic resonance (MR) scans of the brain. Although the absolute
volume of the brain and the frontal lobe was found to be largest in humans, the relative size
of the frontal lobe was similar across hominoids: macaque (28.1%), gibbon (31.1%),
orangutan (35.3%), gorilla (32.4%), chimpanzee (35.9%) and human (36.7%). Most
significantly, it was found that humans do not have a larger frontal lobe than expected from
a primate brain of mankind size (Figure 6.7 and 6.8). Furthermore, the relative size of the
sectors of the frontal lobe (dorsal, mesial, and orbital) was similar across the primate
species studied. Semendeferi and colleagues suggested that the special cognitive abilities
attributed to a frontal advantage may be due to differences in individual cortical areas and
to a richer interconnectivity, none of which required an increase in the overall relative size
of the frontal lobe during hominid evolution.
Figure 6.7. Relative size of the prefrontal cortex in different primates (according to
Semendeferi et al., 1997, 2002).
Schoenemann, Sheehan, and Glotzer (2005) found that a major difference

between humans and other primates was the white matter volume. Using MRI from 11
primate species, the authors measured gray, white, and total volumes for both prefrontal
and the entire cerebrum on each specimen. In relative terms, prefrontal white matter was
found to have the largest difference between human and nonhuman, whereas gray matter
showed no significant difference. Increased brain interconnectivity may represent a major
characteristic of the human brain. As a note of caution, it is important to keep in mind that
subjects used in this study were contemporary people, living in city environments, with a
high level of education, etc., not humans living in those conditions existing 150,000 years
ago. Stimulation can be rather different not only qualitatively but even probably
quantitatively, potentially impacting on brain interconnectivity.
It can be tentatively concluded that it is questionable that the size of the prefrontal
cortex can account for the human executive functions. Some other factors have to be
considered, such as connectivity (increased stimulation?).
Figure 6.8. Volume of the frontal lobe across species. Values include both
hemispheres (according to Semendeferi et al., 1997, 2002).
Executive functions in pre-historical man
Some recent studies have approached the question of the evolution of the prefrontal cortex
and executive functions (Roth & Dicke, 2005; Risberg, 2006; Winterer & Goldman, 2003). It
is usually accepted that Homo sapiens sapiens appeared about 150,000 years ago, and
during this time, his brain evolution has been minimal (Wood, 1992). It means that humans
existing since about 150,000 years ago had basically the very same neurological
organization of contemporary individuals, including the biological foundations for the socalled executive functions.
How were executive functions used by pre-historical man? Of course, we cannot
be sure, but some few papers have approached this question (e.g., Bednarik, 1994, 2003;
Coolidge & Wynn, 2001, 2005; Sugarman, 2002; Wayne, 2006).
Coolidge and Wynn (2001) raised the question of how executive functions
(supposedly, one of the key evolutionary acquisitions that led to the development of modern
thinking) were demonstrated by prehistoric people. Coolidge and Wynn assumed that it is
possible to match many of the features of executive function with activities reconstructed
from archaeological evidence. The potential application of several components of executive
function (such as sequential memory, task inhibition, and organization and planning) is
analyzed by the authors: (1) Sequential memory: it can be speculated in the Palaeolithic
Lithic reduction sequences, but even sophisticated procedures like Levallois can be
explained without resort to closely-linked sequences of action. The production and use of
barbed bone projectile points is another potential marker. The final product depends much
more closely on a set sequence of actions. It is a true multi-step technology. (2) Tasks of
inhibition, in which immediate gratification and action are delayed, are harder to identify
archaeologically. Agriculture requires such inhibition. Facilities such as traps that capture
remotely are technologies of inhibition and were probably present in the European
Mesolithic. Palaeolithic examples are less convincing. Coolidge and Wynn (2001, 2005)
consider that nothing of Middle Palaeolithic foraging, however, would require tasks of
inhibition (indeed, they conclude that nothing in the archaeological record of Palaeolithic
appears to require executive function). (3) Organization and planning is another basic
executive function ability that likely was required for activities such as migration and
colonization.
Coolidge and Wynns (2001) review of the archaeological evidence finds no
convincing demonstration for executive functions among the traces left by Neanderthals.
The authors conclude that the archaeological records support the hypothesis that executive
function was a late and critical acquisition in human cognitive evolution. In a very ingenious
study, Stout and Chaminade (2007) using Positron Emission Tomography (PET) recorded
the brain activity from six inexperienced subjects learning to make stone tools of the kind
found in the earliest archaeological records. The authors found that tool making is
associated with the activation of diverse parieto-frontal perceptual-motor systems, but no
activation was observed in dorsolateral prefrontal cortex. They concluded that human
capacities for sensorimotor adaptation, rather than abstract conceptualization and planning,
were central factors in the initial stages of human technological evolution, such as making
stone tools. Nonetheless, complex cognitive processes (i.e., metacognitive executive
functions) seem to be crucial for further development and survival of Homo sapiens. The
key factor for Homo sapiens late evolution seems to be the mental ability to plan and
strategize, which allowed them to find innovative solutions to the many changing
environmental problems to which they were exposed (Coolidge & Wynn, 2008). This may
be one reason to account why Homo sapiens survived while Homo neanderthalensis
disappeared. Changing environmental conditions (e.g., global climates changes) may
require flexible survival strategies. It has been conjectured that during the past history
changing physical environment conditions resulted in a selection that gave human
ancestors adaptive versatility to endure increasing environmental instability (Bonnefille,
Potts, Chali, Jolly, Peyron, 2004; Potts, 1996, 2004).
Mithen (1994, 1996) has proposed the accessibility of mental modules as the
impetus for mankind culture at the time of the Middle/Upper Palaeolithic transition, about
60,000 to about 30,000 years ago. He identified these mental modules as general
intelligence, social intelligence, natural history intelligence, technical intelligence, and
language. Probably, language was the most important one, increasing communication, and
facilitating the transmission of knowledge, potentially resulting in an increased probability of

survival and reproduction.
It could be speculated that at the beginning of human history, transmitting
knowledge from generation to generation was limited. Although some forms of learning can
be transmitted by modeling or imitation (vicarious learning or social learning or modeling)
(e.g., Bandura, 1977), language development represented a powerful instrument to
accumulate and transmit knowledge about the world. The crucial point in the origins of
executive functions becomes the possibility to conceptualize the environment (concepts are
represented in words) and to transmit and progressively accumulate this knowledge about
the world.
Metacognitive executive functions as a cultural product

There is no convincing evidence that Paleolithic individuals used executive functions
(Coolidge & Wynn, 2001), which can be understood as the ability for planningetc. (first
interpretation of prefrontal abilities: metacognitive executive functions). For thousands of
years, prefrontal abilities were in consequence exclusively used to fulfill basic impulses
following socially acceptable strategies (e.g., hierarchy in the group) (second interpretation
of prefrontal abilities: emotional/motivational executive functions).
Which were the milestones for cultural development and how did metacognitive
executive functions appear? It could be speculated that some crucial inventions fueled the
development of cultural evolution (Vygotsky, 1934/1962). For instance, a kind of cognitive
fluidity has been postulated as a basic requisite for executing complex human activities
(Gardner, 1983). The most important candidate for this crucial invention that fueled the
development of cultural evolution is language. Language allows for the transmission of
knowledge and facilitates survival and reproduction. Without language, children can learn
from parents by imitation, but imitation is limited to some elementary activities, such as
making a simple stone ax. Language represents a major instrument of internal

representation of the world and thinking (Vygotsky,1934/1978). Language development
obviously was a slow process taking thousands of years, but the most critical element of
human language is the use of grammar, likely appearing some 10,000-100,000 years ago
(Ardila, 2006). Probably, Homo neanderthalensis did not have a grammatical language and
according to archeological evidence, did not use executive functions (Coolidge & Wynn,
2008). Language grammar likely developed from action internalization (Ardila, 2006).
Written language represents an extension of oral language. Written language
appeared only some 6,000-8,000 years ago and its diffusion has been so slow that even
nowadays about 20% of the world population is illiterate (UNESCO, 2000). Performance in
psychometric executive function tests has been observed to be very significantly correlated
with subjects educational level (e.g., Ardila, Rosselli & Rosas,1989; Ardila et al., 2000;
Ardila & Rosselli, 2007b; Ostrosky et al., 1998; Reis & Castro-Caldas, 1997; Rosselli et al.,
1990). For instance, Gomez -Perez and Ostrosky-Solis (2006) observed that whereas tests
related to memory are sensitive to aging, those related to executive functioning are mostly
sensitive to education. It can be argued that illiterates possess basic executive functions
(e.g., ability to internally represent actions) but they lack an important instrument to
organize executive functions: written language.
Tentative conclusions
The analysis of executive functions represents one of the most intensively studied
neuroscience questions during the last decade. The emphasis in reasoning, abstracting
skills, behavioral control, anticipating the consequences of behavior, and similar abilities
has contributed to the frequently found false idea that human behavior is guided by
rationality. Human history blatantly contradicts this idea.
This misinterpretation of mankind behavior is linked to the assumptions that the

human brain is unique and superior to the brain of other species. We refer to our species
as the wise man (Homo sapiens). By analyzing executive functions, it may be concluded
that two different types of executive functions could be separated: metacognitive and
emotional/motivational, depending on different brain systems. It could be argued that only
the first one should be referred to as executive functions; usually, however, they are
considered together in most definitions of executive functions, assuming a certain unity.
Contemporary testing of executive functions has focused on abstracting, problemsolving, and similar metacognitive abilities. These metacognitive abilities seem to be useful
in solving external and emotionally neutral problems. When social situations and biological
drives are involved, the ability to rationally solve problems seems to decrease in a
significant way. In this regard, contemporary testing of executive functions has limited
ecological validity.
Archeological analysis has discovered only some if any evidence of
metacognitive executive functions in prehistorical man. We have to conclude that
metacognitive abilities represent a recent acquisition, not obviously dependent on recent
biological changes. The development of some cultural instruments, potentially resulting in a
new type of evolution has been suggested. Language as an instrument not only to
conceptualize the immediate experience, but for its transmission of knowledge, has been
proposed as the major cultural instrument for metacognition. Language complexity has
historically increased with the development of written language. There is no question that
some other cultural instruments have also contributed to the development of metacognitive
abilities; for instance, mathematics, drawing, and technology (from the wheel to
computers). From the point of view of the brain, metacognitive executive functions are not
necessarily correlated with a further brain development; increased neural interconnectivity
may potentially support the increased complexization of executive functions found in
contemporary Homo sapiens.
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7. How we recognize other people?
Introduction
Recognition of own-species members represents a basic survival ability not only for
prehistorical man, but also for every living creature. Lacking this ability, any species would
quickly disappear. Recognition of the own species members is based on a wide range of
multiple sensory information. For instance, insects rely especially on olfactory information to
identify other members of their own species, whereas primates use mainly but not
exclusively visual information (de Waal , 2003; Hinde, 1974; Jolly, 1972; Rssler & Zube,
2010). In mankind, the critical and distinguishing signal features used in the recognition of
other species members have somehow evolved in a parallel way with cultural evolution, as
a result of the use of different clothes, costumes, paintings, hair-styles, make-ups, etc.
People also use a diversity of non-verbal behavior strategies to communicate a given
intention without pre-established conventions (Noordzij et al., 2009).
Paleolithic man most likely lived in small social groups, similar in size to a primate
troop, that is, about 10-100 individuals, composed by one or several couples and their
offsprings (Ridley, 1986); noteworthy, in modern society, we keep affectively living in a
primate-like troop composed by some 10-100 individuals relatives and friendswith whom
we maintain a close affective relationship. Some primitive societies that depend on hunting
and gathering of patchy distributed resources form casual societies not unlike the primate
model (Lee & DeVore, 1968; Wilson, 1975), and the primate model was most likely the first
type of social organization (Van den Berghe, 1979). However, the number of individual
faces that we are potentially able to recognize -"familiar faces", is notoriously over 100, and
probably it can be situated in the order of several thousands.
For the prehistorical man, recognition of other species members was most critical.
According to the living conditions of the prehistorical man, people recognition was suppose
to answer at least two of the following questions: (1) Does the other individual belong to the
same species (i.e., is he/she another Homo sapiens individual)?; (2) what is his/her
gender?; (3) what is his/her emotional state; i.e., is he/she a friend or an enemy? Is he/she
a known (endogroup member; "familiar individual") or unknown (exogroup person;
"nonfamiliar individual") person? And (4) what particular individual is he/she?
Own-species members recognition

Recognition of the own species members does not seem so critical for the contemporary
man, as it was for prehistorical people. However, for people currently living in the
Amazonian jungle and other natural environments, it continues being equally critical as it
was during prehistorical times. It is evident that in Bogot, New York or Paris, the
possibilities to meet a member of another species (for instance, a bear, a lion, etc.) are
quite low. For the prehistorical man, (and it is for a contemporary Tucano Indians living in
the Amazonian jungle) a moving animal supposed the question about what species in
particular it is.
Brain organization of other people recognition has been studied under normal, but
pathological, conditions. Its disturbance is usually known as prosopagnosia (e.g., Bodamer,
1947; Busigny & Rossion, 2009; Damasio et al, 1982). Prosopagnosia can be defined as an
acquired disturbance in the ability to identify familiar faces.
Specialized brain areas involved in face recognition have been studied. Usually, the
damage in the occipito-temporal area, either bilateral (e.g., Bruyer et a, 1983; Damasio et
al, 1982; Ettlin et al, 1992; Meadows, 1974) or right (e.g. Benton, 1990; De Renzi, 1986a;
Landis et al, 1986, 1988; Whiteley & Warrington, 1977) have been associated with
disturbances in face recognition. It is usually assumed that a bilateral occipitotemporal
network mediates face perception (Minnebusch et al., 2009); when this network is
disrupted, face recognition defects are observed.
fMRI procedures have significantly contributed to further our understanding on brain
organization of face perception. It has been found that the brain areas involved in face
recognition include the right middle fusiform gyrus, the left inferior occipital gyrus, and in the
right posterior superior temporal sulcus. The dorsal part of the lateral occipital complex and
the human middle temporal cortex are localized bilaterally (Freeman et al., 2009; Sorger et
al., 2007). Marotta et al., (2001) investigated whether patients with prosopagnosia would
show functional activation in the fusiform gyrus, -the most important brain area usually
regarded as the neural substrate for face processing (Furi et al., 2010)-, when viewing
faces. While the patients did show activation in the fusiform gyrus, with significantly more
voxels in posterior areas than their control subjects, this activation was not sufficient for
face processing. In one of the patients, the posterior activation was particularly evident in
the left hemisphere, which is thought to be involved in feature-based strategies of face
perception, but not in the global recognition of faces. The authors concluded that an
increased reliance on feature-based processing in prosopagnosia leads to a recruitment of
neurons in posterior regions of the fusiform gyrus, regions that are not ideally suited for
processing faces.
Although testing for prosopagnosia is usually carried out using photographs of faces
(Benton et al., 1994; Warrington, 1984), this method obviously represents an extremely
artificial situation. It is interesting to note that untrained people are unable to recognize
individual faces and even everyday objects in photographs. Moldiano et al. (1982) observed
in Mexican Indian children an average error rate of 20% in identifying color paintings of
everyday objects. There is no question that recognition of individuals in photographs
represents a learned and highly trained ability that we usually take for granted. Little
children have a great difficulty to recognize even their own parents and siblings in
photographs. This ability is usually achieved around the age of two years, if adequate
training opportunities are provided (Ellis, 1992).
Face recognition disturbances usually present some specific characteristics: (1)
prosopagnosic patients most often recognize different human races (caucasian, mongoloid,
black), and they can sort human and animal faces (Benton, 1980, 1990; De Renzi, 1986b);
(2) they can also distinguish fruits from flowers, and cars from furniture, although they are
unable to know what specific category member it is (i.e., what particular fruit, flower, car, or
furniture is); (3) prosopagnosic patients usually recognize the general category "human
face" (or "fruit" or "flower), and they can even separate human faces from their
corresponding cartoons (Lopera & Ardila, 1992), but they fail in recognizing the individual
members of the category. These clinical characteristics would suppose the existence of a
highly specialized brain system adapted to recognize own-species members.
Nonetheless, although prosopagnosic patients usually can separate pictures
corresponding to people (own species) from picture corresponding to animals (other
species), they eventually can fail in performing this task (Benson et al., 1974; Bornstein et
al., 1969). This failure supposes an impairment in those specialized own-species brain
detector systems.
Farah et al. (1991) have pointed that the visual recognition of living and nonliving
things can be selectively impaired in cases of brain damage. Patients with prosopagnosia
can present an evident difficulty in recognizing animals and plants; nonetheless, they
usually present a better preserved ability to recognize inanimate objects. A neural system
relatively more important for recognizing living than nonliving things was proposed by the
authors; this system can be selectively impaired by brain damage. Higher visual centers
would be specialized not just to recognize faces, but for the perception of biological forms.
One subsystem of this higher system specialized in the perception of biological forms would
correspond to "human face recognition". Farah et al (1991) point of view in general
supports the perceptual model proposed by Konorski (1967). This perceptual model
postulates the existence of different gnosic brain areas specialized in the recognition of
manipulable and nonmanipulable objects, human faces, emotional facial expressions, and
animated objects. By the same token, in cases of anomia associated with brain damage, it
has been observed that some specific semantic categories can be selectively impaired,
while others are better preserved (Ardila & Rosselli, 2007; Warrington & Shallice, 1984).
This specificity has been also shown in memory (Farah et al., 1989).
Human species members recognize one another basically (although, not exclusively)
based in some visual information. Ethology has carefully studied different species' "sign
stimuli" (Eibl-Eibesfeldt, 1970; Mazur, 2005; Tinbergen, 1951). A sign stimulus refers to
some features of the objects that have been shown to be of major importance in eliciting
responses (Hinde, 1970). The human face evidently could be considered as a "sign
stimulus".
The visual recognition of own species members, as well as the auditory recognition
of own species calls, in several animal species (including mankind) have been shown to be
somehow biologically programmed (Martinez & Matsuzawa, 2009). Some neurons in
different animals' auditory cortex only fire when using the same species calls (Brugge &
Reale, 1985), and probably, this also holds true when visually perceiving members of the
own species (Gross et al, 1972; Rolls, 1984). Perret et al. (1982) found that about 10% of
the neurons they sampled in the superior temporal sulcus of the macaque monkey
selectively respond to faces and not to other stimuli. Desimone et al (1984) found in the
inferior temporal cortex a population of cells that responded selectively to faces. The
responses of these cells were dependent on the configuration of specific face features, and
their selectivity was maintained over changes in stimulus size and position. A particularly
high incidence of such cells was found deep in the superior temporal sulcus. Baylis et al.
(1985) observed that 77% of 44 face-neurons in this temporal area reliably responded more
to some specific faces than to others. Perret et al. (1984) claimed to have found cells that
are peculiarly responsive to a particular human face often seen by the monkey. And
Heywood and Cowey (1992) described cortical neurons that are selectively sensitive to
faces, part of faces and particular facial expressions concentrated in the banks and floor of
the superior temporal sulcus in macaque monkeys. The neurons of the superior temporal
sulcus of monkeys would be, in consequence, part of a system specialized in faces.
Ojemann et al (1992) recorded neuronal activity in adult human subjects and observed that
62% of the studied neuronal populations in the nondominant temporal lobe presented
significant changes in activity during matching of faces and 52% during labeling of facial
emotional expressions. These results would support the specificity of a highly specialized
neuronal face-recognition brain system.
Although the overwhelming majority of cases of prosopagnosia reported in the

literature presented in addition to the face recognition impairments, some associated
deficits in the recognition of individual members belonging to other visual categories (most
often, living things -fruits, flowers, etc., but also nonliving things -buildings, cars, furnitures,
etc.) prosopagnosia can be occasionally restricted only to the recognition of faces (De
Renzi, 1986; De Renzi et al, 1992; Farah, 1990). Conversely, there are patients with severe
visual agnosia for real objects without any evident defect in face recognition (Feiberg et al.,
1986; Hecaen & Ajuriaguerra, 1956). Furthermore, prosopagnosic patients can be able to
perform very complex perceptual tasks and can perceive and recognize many stimuli that
are visually more complex than human faces (Benton & Van Allen, 1972; Busigny et al.,
2010; Damasio, 1985). This supposes specificity in face recognition defects.
Busigny et al. (2010) tested a prosopagnosic patient in three delayed forced-choice
recognition experiments in which visual similarity between a target and its distractor was
manipulated parametrically: novel 3D geometric shapes, morphed pictures of common
objects, and morphed photographs of a highly homogenous familiar category (cars). In all
experiments, the patient showed normal performance and speed, and there was no
evidence of a steeper increase of error rates and RTs with increasing levels of visual
similarity when compared to controls. According to the authors, these data rule out an
account of acquired prosopagnosia in terms of a more general impairment in recognizing
objects from visually homogenous categories. They assume that overall, these
observations allow for the conclusion that brain damage in adulthood may lead to selective
recognition impairment for faces, perhaps the only category of visual stimuli for which
holistic/configural perception is not only potentially at play, but is strictly necessary to
individualize members of the category efficiently.
In conclusion, it seems reasonable to suppose the existence of some brain neuronal
subsystems specialized in the recognition of own-species members. These subsystems
would participate in a higher neuronal system specialized in the recognition of biological
forms. Individual members (individual faces) would be encoded into the "face recognition
subsystem". The record of neuronal activity would affirm the existence of highly specialized
neuronal subsystems involved in the perception of faces (Desimone et al, 1984; Gross et
al, 1972; Heywood & Cowey (1992); Ojemann et al, 1992; Perret et al, 1982; Righart et al.,
2010; Rolls, 1984).
Gender recognition
Gender recognition (filognosis; from the Greek, filo = gender) represents a crucial
perception that will define further social behavior (100,000 years ago, and even nowadays).
Taking into account that in mankind a moderate sexual dimorphism exists (females usually
have an average smaller height and possess sexual signals that can be easily recognized
either by the front or by the back; additionally, gait is different), it is easy to suppose that
visual signals were for the pre-historical man, and continue being for contemporary man,
relevant and effective (Morris, 1977). Furthermore, not only body configuration but also
male's and female's clothes are quite different and identifiable in their construction, shape,
and even colors. Some female primates have areas of "sexual skin" which swell and/or
change in color with changes in the reproductive state of the animal (Hinde, 1974)
representing an evident visual identification mark.
Prosopagnosic patients may be unable to identify male and female faces (Bruyer,
1986; Damasio et al., 1990; Lopera & Ardila, 1992), and it can be proposed that they will
also present general defects in recognizing males and females according to other (not
facial) sexual signals. They can also present kind of whole-body recognition defect. Indeed,
in prosopagnosia a defect not only in face but also in body perception can be found
(Righart & de Gelder, 2007). The prosopagnosic patient described by Bauer (1982) decided
to cancel his subscription to the journal Playboy after becoming prosopagnosic; Bauer
suggested the possibility that his patient could present an agnosia for individual nudes,
analogous to the defect in the recognition of individual faces. Conversely, the author of this
paper studied a prosopagnosic patient with a virtually complete inability to recognize any
face, and even to sort males and females faces. However, he easily and accurately
distinguished male and female bodies. This implies that facial and whole-body
males-females distinction can become dissociated. Or at least, that body recognition can be
preserved, while face recognition is impaired. If this last assumption were true, it would
imply a "sensitivity hierarchy": it is easier (and better preserved in brain-damaged patients)
to recognize males-females using whole-body than facial signals.
The idea that gender differences aid in the ability to recognize human faces has
been suggested. Ino et al. (2010) performed a fMRI experiment in which participants
encoded and recognized male and female faces. Behaviorally, the facial recognition ability
of men and women was similar and was superior for female faces compared to male faces.
At the neural level, widespread areas showed greater responses for men vs. women during
the encoding and recognition phase, and several areas, including the hippocampal region,
showed greater responses to female vs. male faces during recognition. The authors
proposed that the reduced activation of women's brains during encoding and recognition
suggests that the relevant neural systems were more efficiently recruited in women than in
men.
Noteworthy, visual signals are not the only ones used in gender recognition: there
are also auditory signals resulting from a different voice timbre, and additionally, distinctive
olfactory signals. Auditory and olfactory signals are probably more readily used in low
illumination conditions, while visual signals are easily available in daytime conditions.
These visual, auditory, and olfactory gender signals remain in our contemporary
mankind members, despite the differences in cultural backgrounds. Visual marks have not
changed, although usually they can be covered. Height differences remain, although
women may use higher shoes for increasing their heights. The differences in gait are
evident. Voice-timbre differences supposedly have not changed during the last 150,000
years. And olfactory signals can be artificially covered and replaced by other new olfactory
signals, but anyhow they remain as gender marks.
Olfactory recognition deserves some special consideration. Olfactory communication
plays a crucial communication role in most animals, including primates (Hinde, 1970; Jolly,
1972; Mundy, 2006). Very often, sexual behavior is partially under olfactory control: a
pheromone is produced that acts as a powerful attractant to the male (Hoover, 2010). The
tendency of women living together to menstruate simultaneously may be mediated by
olfactory stimuli (Carlson, 2009). A male pheromone is detected most easily by women of
reproductive age, but men can smell it if given oestrogen; and olfactory threshold have
been observed to vary during the menstrual cycle (Conform, 1970; Hinde, 1974;
Eibl-Eibesfeldt, 1970). So, olfactory signals continue being effective in gender identification.
Perfumery industry has become a solid and well-established enterprise.
In summary, gender identification can be mediated by different types of signals:
facial, whole-body, and even auditory and olfactory signals.
Emotional expression and emotional recognition

Some basic emotional expressions are universals and can be easily recognized by any
member of any culture (Ekman, 1972; Kohler et al., 2004). Aggressive gestures, protective
gestures, threatening signals, submissive postures, and sexual approach signals are
roughly identical in any cultural group, and they are quite similar to those observed in
non-human primates (Eibl-Eibesfeldt, 1970; Morris, 1977). It can be supposed that they
existed in a similar form in the pre-historical man. Some other emotional expressions
present major or minor variations across different cultural groups. Surprise, joy, mourning,
etc., can present important cross-cultural differences. Special ornaments are often used to
make a special emotional state even more easily identifiable: aggression, sexual interest,
mourning, etc. (Ekman, 1972; Eibl-Eibesfeldt, 1973).
During child development, the face represents the earliest visual stimulus capable to
release an emotional response (Fantz, 1961). Facial identification and emotional
recognition can be dissociated in brain-damaged individuals. In some cases of
prosopagnosia the recognition of facial expression can be preserved while face
identification is impaired (Bates et al., 2009; Bruyer et al., 1983; Shuttleworth et al., 1982).
Conversely, some brain-damaged patients can preserve the ability to identify faces, but fail
in recognizing facial emotional expressions. Most often, right hemisphere-damaged patients
present serious difficulties to identify, match and comprehend emotional expressions
(Feyereisen, 1986). Kurucz and Feldmar (1979) found that some patients could recognize
photographs of famous faces, but they were unable to identify their facial expressions. By
the same token, the patient reported by Lopera and Ardila (1992) did not recognize facial
emotional expressions, but usually was able to deduce them (e.g., "This must be a smiling
and joy face, because the teeth are seen through the mouth").
It becomes plausible that facial identification and the recognition of emotional
expressions depend on, at least partially, different brain subsystems (Peelen et al., 2009;
Stephan & Breen, Caine, 2006). Thus, two different visual agnosic syndromes could be
found in brain-damaged patients: agnosia for faces (prosopagnosia) and agnosia for
emotional expressions (prosopo-affective agnosia). Konorski (1967) proposed the
existence of different brain systems (different "gnostic areas") to recognize human faces
and to recognize emotional facial expressions. Recently it has been shown that whereas
face recognition defects are associated with cortical damage (very specially, the right
fusiform gyrus) the recognition of the facial expression of emotion depends on white matter
association tracts, very specially the inferior fronto-occipital fasciculus (Philippi et al., 2009).
Etcoff (1984) postulated the existence of different "modules" for the visual
identification of faces and facial expressions. She observed that the speed and accuracy
with which normal subjects perform a sorting task (to put photographs of faces in different
piles according to either their identity or their expression) is not affected by whether facial
identity is correlated with facial expression, implying that these two proprieties of faces are
processes independently. Etcoff postulated that two separate brain modules underlie the
recognition of facial identity and facial expression but that they are neuroanatomical
neighbors.
It has also been shown that prosopagnosic patients can retain some covert
recognition of faces. These patients present a physiological response for familiar, but not
for unfamiliar faces (Barton et al., 2001; Bates et al., 2009; Bauer, 1984; De Haan & Young,
1987; De Haan et al, 1992; Tranel & Damasio, 1985; Young & De Haan, 1988). By the
same token, in associative learning tasks, performance is better if familiar faces are used
(Bruyer et al., 1983). These findings suggest that despite unawareness in face recognition,
some covert face recognition can remain in prosopagnosia syndrome. However, this not
surprising at all. Everyday experience discloses that very often, when seeing a particular
face, we can be totally unable to identify who he/she is, despite having the "feeling" that we
really know that particular individual; we simply have a "feeling of familiarity". The
recognition of the individual member can be impossible in this everyday experience (and
can be impaired in cases of brain-damage), but the distinction "familiar" and "not familiar"
remains.
Valds-Sosa et al. (2011) observed in a prosopagnosic patient face-selective
activations bilaterally in his occipital gyri and in his extended face system (posterior
cingulate and orbitofrontal areas), the latter with larger responses for previously-known
faces than for faces of strangers. In the right hemisphere, these surviving face selectiveareas were connected via a partially persevered inferior fronto-occipital fasciculus.
According to the authors, this suggests an alternative occipito-frontal pathway, absent from
current models of face processing, that could explain the patient's covert recognition while
also playing a role in unconscious processing during normal cognition.
Individuals' recognition
Endogroup members are usually very alike (resulting from endogamy) in their height, body
contexture, skin color, and additionally, in the clothes and make-up they wear. Usually, they
can be visually identifiable even at long-distances.
Erroneously, we have learned that individuals are recognized just by their faces. This
can be partially true in our urban societies, where we have very limited possibilities to
perceive other individual characteristics (e.g., his/her body configuration, his/her gait, etc).
In a survey of 1,000 peoples photographs (excluding commercial announcements)
randomly taken from the two most influential newspapers and the two most influential
magazines in Colombia, it was found that face photographs were about four times more
frequently published than whole-body photographs. Evidently, we are over trained in
individuals' recognition relying only on facial cues. However, facial information is quite
insufficient to recognize individuals for anybody living in rural areas, in open fields or in
savannas. People living in Argentinean Pampa or Paraguayan Chaco easily recognize
approaching or passing-by people when they are still 500 meters or farther away. They do
not depend, of course, solely upon face recognition to identify individuals (face can be
recognized only within very short distances) but upon a broader diversity of signals, such as
body configuration, gait, and even clothes. The human brain should possess not simply a
system for encoding and memorizing faces (prosopognosis) but also for encoding and
memorizing body configurations and general personal features (by the way, "prosopos" in
Greek means not only face, but also person, and prosopagnosia should be understood as
the inability to identify not simply faces, but persons).
Thus, recognition of individuals and recognition of faces is not equivalent. The face
is only one of the visual characteristics used to recognize individuals, but it is not the only
one, and eventually, it was not the most important one for the prehistorical man (or for the
current jungle inhabitants, for the inhabitants of the Argentinean Pampa or for army
members), although evidently it is the most important one in our current city-living
conditions. It could be conjectured that that in addition (or superimposed) to the ability to
recognize faces, the human brain should possess an ability to recognize individual body
configurations and body marks. Furthermore, faces yield information not only about the
individual, but also (and eventually even more importantly) about his/her specific emotional
state. By the same token, in everyday conditions, faces are not static but continuously
moving. Interestingly, prosopagnosic patients may recognize faces on the basis of their
idiosyncratic facial movements (Steede et al., 2007).
To identify individual members one should be able to recognize body marks and
general configuration (somagnosis, that is, body recognition), and face signals
(prosopognosis). Patients with prosopagnosia cannot discriminate individuals members in a
group, but they can use sufficiently evident visual marks (e.g., a face with wrinkles means
that it should correspond to an elderly person; a face with a beard should correspond to a
male, etc).
Somagnosis has not been systematically analyzed in neuropsychology yet.
Furthermore, it does not seem easy, considering that currently the most important body
marks are the clothes (changing from one day to another), although it seems evident that
some people possess a tremendous ability to identify individuals by their clothes. Our
knowledge about other people's body configuration is in most cases just approximate.
However, it is evident that in addition to memory for people's faces, we also have some
memory for people's height, contexture, gait, etc. It is reasonable to suppose that patients
presenting face recognition deficits may also present body recognition defects.
Interestingly, patients with prosopagnosia usually also present difficulties recognizing
animals, either animal faces or whole body recognition (Farah, 1989). Damasio et al (1982)
reported a prosopagnosic patient with difficulties to identify people's gaits, but usually
patients with prosopagnosia are not tested in recognizing people when using diverse visual
characteristics, such as body configuration and gait.
Different anatomical substrates have been suggested for the recognition of familiar
and nonfamiliar faces (Warrington & James, 1967). Nonaphasic patients with right posterior
lesions present the most remarkable difficulty in discriminating familiar faces. Lopera and
Ardila (1992) proposed further to distinguish two different neuropsychological syndromes:
prosopagnosia (as a more or less isolated perceptual defect in face recognition), and
prosopamnesia (as a memory defect for faces). In the first case (prosopagnosia) right
occipital-temporal damage would be sufficient; prosopamnesia would be associated with
bilateral lesions. Individuals' face recognition would correspond to the specific elements (or
items) of this "familiar faces" subsystem. De Renzi et al (1991) introduced a similar
distinction and separated two forms of prosopagnosia: apperceptive (as a disorder in face
identification), and associative (as amnesia for faces) forms of prosopagnosia. Wilkinson et
al. (2009) observed that unilateral damage to the right cerebral hemisphere disrupts the
apprehension of whole faces and their component parts.
Barton (2008) proposed that, (1) prosopagnosia is more severe with bilateral than
unilateral lesions, indicating a minor contribution of the left hemisphere to face recognition,
(2) perception of facial configuration critically involves the right fusiform gyrus and (3)
access to facial memories is most disrupted by bilateral lesions that also include the right
anterior temporal lobe. According to the author, this supports assertions that more
apperceptive variants of prosopagnosia are linked to fusiform damage, whereas more
associative variants are linked to anterior temporal damage. It has been also further
suggested that (a) the most specific forms of prosopagnosia are due to lesions of a right
posterior network including the occipital face area and the fusiform face area, whereas (b)
the face identification defects observed in patients with left temporo-occipital lesions seem
due to a semantic defect impeding access to person-specific semantic information from the
visual modality. Furthermore, face recognition defects resulting from right anterior temporal
lesions can usually be considered as part of a multimodal people recognition disorder
(Gainotti, G. & Marra, 2011).
Probably, we have learned to identify faces in the same way that an ornithologist has
learned to identify birds or a farmer to identify individual animals. Some reports point to the
possibility of a prosopagnosic deficit restricted to a very specific visual subcategory. Assal
et al. (1984) reported a case of a peasant devoted to caring for cows with a restricted
agnosia for cows, associated with a transient prosopagnosia for human faces, anterograde
and retrograde amnesia, and topographic amnesia. The patient had difficulty in visual
imagery for cows but not for other visual categories, and visual hipoemotionality for cows
faces ("the cows have lost their personality and colorfulness"). This case of restricted
zooagnosia supports the specificity in learned visual recognition of individuals within a
particular visual subcategory. Difficulties in recognizing faces belonging to a different racial
group are well known to everyone, whereas twins are easily and errorless recognized by
their own parents and siblings.
It has been suggested that prosopagnosia arises due to an impairment of a process
that reduces uncertainty about the nature/location of the diagnostic cues for face
individualization: the ability to perceive multiple elements of a face as a single global
representation (holistic processing) (Ramon & Rossion, 2010). Being impaired at

processing individual faces holistically, prosopagnosic patients would tend to perform
relatively worse for processing facial areas containing multiple elements (i.e., the eyes),
and for elements that are widely spaced apart.
Prosopagnosic patients usually recognize people when hearing their voices (e.g.,
Bodamer, 1947; Damasio et al., 1982). Voice recognition disorders impair the ability to
recognize individuals. Phonagnosia has been defined as the acquired inability to recognize
and discriminate voices (Van Lancker & Carter, 1982). A further distinction has been
introduced between the discrimination of familiar and unfamiliar voices (Van Lancker et al.,
1988; Van Lancker et al., 1989). Deficits in recognizing familiar voices are significantly
correlated with damage to the inferior and lateral parietal regions of the right hemisphere,
whereas impairment of voice discrimination abilities is associated with temporal damage to
either hemisphere. This distinction clearly parallels the distinction between prosopagnosia
and prosopamnesia (Lopera & Ardila, 1992) (or between apperceptive and associative
prosopagnosia). It is important to point out that voices (like faces) also convey emotional
information. Occasionally, only auditory (but not visual) information is used to recognize a
particular individual (e.g., by phone).
A whole array of neuropsychological syndromes could have been associated with
defects in the recognition of individuals: some types of visual agnosia (prosopagnosia,
afilognosia, asomagnosia), deficits in voices recognition (phonagnosia), and even
eventually, disturbances in smell perception (hiposmia, anosmia, and potentially
osmagnosia).
In summary, it can be proposed that people recognition is based, predominantly but
not exclusively, in some visual information. Different subsystems or modules can be
distinguished. A first level analysis implies separating living (people, animals, plants) from
nonliving things (furnitures, cars, etc). Individual identification supposes the distinction of
familiar and nonfamiliar individuals. Additionally, gender and emotional states are to be
recognized in order to achieve a unitary individual perception.
Conclusions
A great effort has been devoted in neurology and neuropsychology to the analysis of face
recognition under normal, and specially, under pathological conditions. However, cultural
differences in people recognition show that, not only facial perception can be relevant in
individuals' identification, but also other visual signals, such as body and gait
characteristics. Furthermore, not only visual information may be relevant for people
recognition; auditory and even olfactory information can be also important in people
identification. Visual information can be more important in daylight conditions, while
auditory and olfactory signals can become relevant in dim conditions.
In cases of brain damage, sometimes one category or type of information can be
preserved, whereas others are impaired. At least the following perceptual dissociations
have been observed in brain-damaged patients:
1. Perception of living and non living things (Farah et al., 1991);
2. Perception of own-species and other species members; that is, people and
animals (e.g., Benton, 1980, 1990; De Renzi, 1986; Farah, 1990);
3. Perception of familiar and nonfamiliar faces (e.g., Bauer, 1984; De Haan &
Young, 1987; De Haan et al., 1992; Lopera & Ardila, 1992; Warrington and James, 1967);
4. Face identification and recognition of emotional expressions (e.g., Bruyer et al.,
1983; Feyereisen, 1986; Shuttleworth et al., 1982);
5. Facial gender-identification and whole-body gender-identification (Ardila &
Rosselli, unpublished); and
6. Visual and auditory people recognition (e.g., Bodamer, 1947; Van Lancker et al.,
1988; Van Lancker et al., 1989);
Different subsystems (or "modules") could be involved in people recognition.
"People" could represent a subsytem included within the higher level "living things"
system. One subgroup of this "people" subsystem includes "familiar individuals" (versus
"nonfamiliar individuals"). "Familiar individuals" includes all the stock of known people,
perhaps, several thousands. Face can be enough to recognize an individual (although
voice, gait, body configuration signals, etc., can be also enough to recognize the very same
individual). Additionally, gender and emotional expression are conferred to familiar, but also
to nonfamiliar persons. Gender and emotional expression can be recognized not only
departing from visual, but also auditory information. Individual's recognition represents the
final step in this people processing system. Individual's recognition (as it is the meaning of
a particular word) represents a complex perception, including multiple association systems
(especially visual, but also auditory and even olfactory), and maintaining some specific
emotional, memory, and even verbal (individual's name) relationships.
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8. Culture and Cognitive Testing4
Introduction
In neuropsychology, cognitive disturbances associated with brain pathology of a limited
subsample of the human species --contemporary Western, and most often, urban
middle-class and literate brain-damaged individuals-- have been relatively well analyzed.
Our understanding about the brain's organization of cognitive abilities, and the disturbances
in cases of brain pathology, is therefore not only partial but, undoubtedly, culturally biased
(Ardila, 1995; Fletcher-Janzen, Strickland & Reynolds, 2000; Uzzell, Pontn & Ardila,
2007).
Cultural and linguistic diversity is an enormous, but frequently overlooked,
moderating variable. Several thousands of different cultures have been described by
anthropology (e.g., Bernatzik, 1957; Rosaldo, 1993), and contemporary humans speak
over 6,800 different languages (Grimes, 2000; www.ethnologue.com). Norms for
performance in a sufficiently broad array of neuropsychological tests and an extended
analysis of cognitive disturbances in different cultural and ecological contexts are
necessary for us to understand the brain organization and evolution of cognition.
A significant interest in understanding cultural variables in neuropsychology has
been observed since the 1980s and particularly since the 1990s (e.g., Ardila, 1993, 1995;
Boivin & Giordani, 2009; Chen et al., 2009; Choudhury et al., 2010; Ferraro, 2002; FletcherJanzen et al., 2000; Nell, 2000; Rendell et al., 2011; Uzzell et al., 2007).
Different questions have been approached including but not limited to: Bilingualism
research; historical origins of cognition; studies on illiteracy; cross-linguistic analysis of
4 A previous version of this chapter was published in: Uzzell, B., Pontn, M. & Ardila A. (eds). (2007). International
Handbook of Cross-Cultural Neuropsychology. Mahwah, NJ: Lawrence Erlbaum Associates, pp. 23-45
aphasia, alexia and agraphia; research about the influence of socioeducational factors in
neuropsychological performance; norms in different national and cultural groups; studies on
cultural variables on handedness; neuropsychological assessment and treatment in diverse
human groups; analysis of neuropsychological test bias; cultural application of different
neuropsychological test batteries; legal and forensic significance of cultural factors; and
cognitive abilities in different cultural contexts.
In this chapter, an attempt will be made to summarize the major cultural variables
affecting cognitive test performance. I will attempt to integrate some ideas previously
presented in different publications (Ardila, 1993, 1995, 1996, 1999, 2003, 2007; Ardila et
al., 2000a, 2000b, 2010; Ardila, Rodriguez & Rosselli, 2003; Harris et al., 2001; Ostrosky
et al., 1998; Puente & Ardila, 2000).
What is culture?
Culture refers to the set of learned traditions and living styles, shared by the members of a
society. It includes the ways of thinking, feeling and behaving (Harris, 1983). The minimal
definition of culture could simply be, culture is the specific way of living of a human group.
Three different dimensions of culture can be distinguished: (1) The internal,
subjective or psychological representation of culture, including thinking, feeling, knowledge,
values, attitudes, and beliefs. (2) The behavioral dimension, including the ways to relate
with others, ways of behaving in different contexts and circumstances, festivities and
meeting, patterns of associations, etc. (3) Cultural elements: the physical elements
characteristic of that human group such as symbolic elements, clothes, ornaments, houses,
instruments, weapons, etc.
Culture represents a particular way to adapt to and survive in a specific context.
Cultural differences are strongly related with environmental differences. Eskimo and
Amazonian jungle culture differences are in a significant extent due to the geographical and
environmental differences between the Arctic region and the Amazonian jungle. Cultures,
however, are usually in some contact and a significant cultural diffusion is generally
observed. Cultural evolution and cultural changes are found throughout human history,
depending upon, (a) new environmental conditions, (b) contact with other cultures, and (c)
internal cultural evolution. For example, Gypsies in Russia and Gypsies in Spain have
many cultural commonalties, but also many differences.
Cultures can be grouped into branches using different criteria, but mainly, their
origins (e.g., Latin cultures, Anglo-Saxon cultures, Islamic cultures, Amerindian cultures,
etc.). When comparing two cultures, certain relative distance could be assumed. For
instance, the cultural distance between Mediterranean cultures and Anglo-Saxon cultures is
lower than the cultural distance between the Mediterranean cultures and the Amerindian
cultures. This means that Mediterranean people have more attitudes, beliefs, behaviors,
and physical elements in common with Anglo-Saxons than with Amerindians.
Certain cultural elements have been particularly successful and have tended to
strongly diffuse across cultures. For instance, science and technology have been extremely
successful in solving different human problems and have, in consequence, tended to
spread throughout virtually all-existing worldwide cultures. In this regard, contemporary
man has tended to become more homogeneous and to share the culture of science and
technology. To live in Peking and New York is not so different today as it was living in
Tashkent and Rome several centuries ago. Furthermore, communication is faster today
than it was anytime in history and cultural diffusion has become particularly fast.
Formal education and school have played a crucial role in the diffusion of science
and technology and in the contemporary trend toward the relative cultural homogenization.
In this regard, school can be considered as a subculture, the subculture of school (Ardila,
Ostrosky & Mendoza, 2000). School not only provides some common knowledge but also
trains some abilities and develops certain attitudes. Cognitive testing is obviously based on
those assumptions as well as values of scientific and technologically-oriented societies.
Schooled children usually share more scientific and technological values and attitudes than
their lower educated parents, and schooled subjects significantly outperform illiterate
individuals in cognitive testing (e.g., Ardila et al., 2010; Ostrosky, Ardila, Rosselli,
Lpez-Arango & Uriel-Mendoza, 1999; Reis, Guerreiro & Petersson, 2003; Rosselli, 1993).
Why culture affects cognitive test performance?

Cross-cultural cognitive testing has been a polemic matter because cognitive assessment
uses certain strategies and elements that are not necessarily shared by every culture
(Laboratory of Comparative Human Cognition, 1983). Greenfield (1997) has pointed out
that there are three different reasons to account why cognitive ability assessments do not
cross cultures: (1) Values and meanings, (2) modes of knowing, (3) and conventions of
communication.
Values and meanings means that there is not a general agreement on the value or
merit of particular responses to particular questions. For example, some people may
consider that in the Ravens Progressive Matrices test, it is a better answer that one
following an aesthetic principle (i.e., the figure that looks better in that position) than the
one according to a conceptual principle (i.e., the figure that continues the sequence).
Furthermore, the same items do not necessarily have the same meaning in different
cultures, regardless of how appropriate and accurate the translation is. An item referring to
the protection of animals may have a rather different meaning in Europe than in a hunting
society. The question Why should people pay taxes? may trigger quite different
associations in a society where people consider that taxes are fairly expended than in a
society where people think that taxes are misused.
Knowing may be a collective endeavor and not an individual task. Many collective
societies find it surprising that the testing situation requires individuals responses without
the participation of the social group. If most activities are carried out in a collective way,
why should answering a test be the exception? Many cultures, on the other hand, do not
make a distinction between the process of knowing and the object of knowing. In
consequence, questions such as why do you think?, or why do you consider? may be
incomprehensible. The point is not what I think or I consider; the point is how it is.
Conventions of communication are highly culture-dependent. The test questions
assume that a questioner who already has a given piece of information can sensibly ask a
listener for the same information. To ask or to answer questions can be highly variable
among cultures. American children, for example, learn that they should not talk to
strangers, but they also learn that they should answer questions to the doctor, regardless
that the doctor is a stranger. In many societies adults rarely talk with children (What could
you talk about with a child?), and it is not considered appropriate for children to participate
in adults conversations. Furthermore, relevant information is not always the same in every
culture. Many types of questions can be difficult to understand. To copy nonsense figures
(e.g., Rey-Osterrieth Complex Figure) can be suspicious for many people. It may be a
relevant item for an American school child, but it is absurd for somebody living in a nonpsychometrically oriented society. Certain question formats used in testing can be
unfamiliar or less familiar in many cultures. For instance, after his first multiple-choice test,
a college Haitian student in the US returned it to the instructor pointing out I simply do not
have the minimal idea of what I am supposed to do. Conversely, I have found that
American university students score notoriously lower in open-question exams than in
multiple-choice formats.
Effect of culture is not limited to verbal abilities, but is also clearly found on
nonverbal abilities too (Rosselli & Ardila, 2003). When nonverbal test performance in
different cultural groups is compared, significant differences are evident. Performance on
non-verbal tests such as copying figures, drawing maps or listening to tones can be
significantly influenced by the individuals culture.
Five different cultural aspects potentially affecting neuropsychological test
performance will be emphasized: (1) patterns of abilities, (2) cultural values, (3) familiarity,
(4) language, and (5) education.
Patterns of abilities
While basic cognitive processes are universal, cultural differences in cognition reside more
in the situations to which particular cognitive processes are applied than in the existence of
the process in one cultural group and its absence in the other (Cole, 1975). Culture
prescribes what should be learned, at what age and by which gender. Consequently,
different cultural environments lead to the development of different patterns of abilities
(Ferguson, 1956). Cultural and ecological factors play a role in developing different
cognitive styles (Berry, 1979).
Cognitive abilities usually measured in neuropsychological tests represent, at least in
their contents, learned abilities whose scores correlate with the subject's learning
opportunities and contextual experiences. Cultural variations are evident in test scores, as
culture provides us with specific models for ways of thinking, acting and feeling (Ardila,
1995; Berry, 1979).
Cultural values
Culture dictates what is and what is not situationally relevant and significant. What is
relevant and worth to learn or to do for an Eskimo does not necessarily coincide with what
is relevant and worth learning or doing for an inhabitant of the Amazonian jungle. A culture
provides specific models for ways of thinking, acting and feeling, and cultural variations in
cognitive test scores are evident (Anastasi, 1988).
Current neuropsychological testing uses specific conditions and strategies that may not
be only unfamiliar to many people, but also may violate some cultural norms. At least the
following cultural values underlay psychometrically oriented cognitive testing (Ardila, 2005):
1. One-to-one relationship. There is a tester and there is a testee. Hence, it is a oneto-one relationship between two people that very likely have never met before, are
aliens, and will not meet again in the future.
2. Background authority. The testee will follow (obey) the instruction given by the
tester, and hence, the tester has a background or situational authority. It is not so
easy, however, to understand who and why this authority was conferred.
3. Best performance. The testee will perform at best. Performance at best is only
done in those endeavors that are perceived and regarded as extremely important
and significant. It is supposed in consequence that the testee has to perceive testing
as a most important and significant endeavor. It may not be clear enough in many
cultural groups why it is so important and relevant to repeat a series of nonsense
digits or to draw an absurd figure.
4. Isolated environment. Testing is done in an isolated room. The door is closed and
even locked. Usually, nobody else is allowed to be present, and in this regard it is a
private and intimate situation. Private appointments with aliens may be quite
inappropriate in many cultures. The testee has to accept this type of unusual social
relationship.
5. Special type of communication. Tester and testee do not maintain a normal

conversation. Tester uses a stereotyped language, repeating over and over again
the same phrases in a rather formal language. Testee is not allowed to talk about
him/herself. Nothing points to a normal social relationship and usual conversation.
This is a type of relationship that can be different from any type of relationship
existing in the subjects past experience. For Hispanics, as an example, the personal
relationship with the examiner may be more important than the test results
(Geisinger, 1992). Dingfelder (2005) points out that The detached professional
relationship that many therapists cultivate with their clients may seem alien to those
Latinos that adhere to the value of close interpersonal relationship. Therapist might
consider sharing some minor details of their lives with these clients, to make the
clients feel more comfortable and welcome (p. 59).
6. Speed. In many tasks the tester warns that the testee must perform as fast as
possible and even time is measured. In the middle of the task, however, the tester
frequently interrupts saying, stop! For many cultural groups speed tests are frankly
inappropriate. Speed and quality are contradictory, and good products are the
results of a slow and careful process. Speed, competitiveness and high productivity
are most important cultural values in literate Anglo-American society, but that is not
true in other cultural groups.
7. Internal or subjective issues. The tester may ask questions that can be perceived
as a violation of privacy. Questions about cognitive issues (e.g., How is your
memory?) are also questions about internal subjective representations, the most
personal private sphere. Frequently, intellectual or cognitive testing may be
perceived as aversive in some cultures. In Latin America, usually highly educated
people dislike and try to avoid cognitive testing. Intellectual testing may even be
perceived as kind of humiliating situation and disrespect to the privacy.
8. Use of specific testing elements and testing strategies. The tester uses figures,
blocks, pictures, etc., and the reason for presenting them may not be easy to
understand. That is, the reason may be evident for the tester (e.g., to assess
memory) but not for the testee. Sometimes the tester explains that it is like a game,
but there is no evident reason to come to play with this alien tester. Sometimes the
tester refers to exercises, but exercises are by definition useless activities without
any evident goal. Exercises are indeed preparation for something. Preparation for
what? Furthermore, it they are just exercises why to perform at best? In brief, it is
not easy to understand (and to explain) the reason to memorize meaningless digits
or saying aloud as many animal names as possible in one minute, etc.
In summary, the rationale and the procedures used in cognitive testing rely on a whole
array of cultural values that in no way can be regarded as universal values. When testers
use tests developed in their own culture to test members of a different culture, testees often
do not share the presumptions implicitly assumed by the test (Greenfield, 1997; p. 1115). It
is not surprising that the members of the culture where the test was developed usually
obtain the highest scores.
Familiarity
Familiarity with the testing situation includes not only the elements used in testing (bikes,
houses, figures, stories, etc.) but also the testing environment (see above), and the cultural
relevance (meaningfulness) of the elements of the test (Ardila & Moreno, 2001). Familiarity
also refers to the strategies needed to solve the task and the attitudes required to succeed.
Competitiveness, for example, in many societies is viewed with suspicion. Cooperation and
social ability may be far more important.
The Boston Naming Test (even the version adapted in Spain) includes naming a
beaver and an acorn, an animal unfamiliar for people living in South America and a virtually
unknown plant. North American people very likely would consider it unfair to be tested by
naming South American animals and plants. The Boston Naming Test also includes a
pretzel, a most typical American element but totally unknown in most countries. Obviously,
it would also be frankly unfair to test naming ability in American subjects using tortillas or
tacos as stimuli. Figures representing snow may be unfamiliar for people living in tropical
and sub-tropical areas.
Cultural relevance (meaningfulness) may be another significant confounding factor in
cross-cultural neuropsychological testing. Items developed in a particular cultural context
do not have the same relevance when translated to another culture. Spelling out words
(frequently included in the Mini-Mental State Exam) is not used in languages with
phonological writing systems (such as Russian, Italian or Spanish), and hence it is
perceived as an artificial task. In many world cities, people get oriented using cardinal
points (North, South, West, and East) but in no way is this strategy found in every culture. I
personally do not know where is North, South, West, and East in my Colombian hometown
simply because I never used it. People in Barcelona (Spain) use to spatial directions:
toward the sea and toward the mountain. People in Colombia frequently use up and
down, referring to the numbering system, but up and down in Guadalajara (Mxico)
mean from downtown and toward downtown. The Picture Arrangement subtest from the
Wechsler Intelligence Scale may have different levels of difficulty in different cultural
contexts, depending on the familiarity with the storys elements. Something may be obvious
in a culture, but unusual and weird in another.
Language
Language plays an instrumental role in cognition (Vygotsky, 1962, 1989). As a matter of
fact, it represents the major cognitive instrument. Different languages differ in phonology,
lexicon (semantic field of the words), grammar, pragmatic, and reading systems. These
differences may affect language test performance. Different languages conceptualize the
world in a different way (Whorf, 1956). For instance, the notion of time is quite different in
Latin languages than in Germanic ones. Latin languages have a significantly high number
of tenses pointing to some temporal nuances. Slavic languages use perfective and non
perfective tenses in verbs. Space and casualty are also coded different in different
languages.
Language usage differs according to the cultural (and subcultural) background and
strongly correlates with the subject's educational level. Sometimes, test instructions (and in
general, the language used in testing) are given in a formal language, which may be very
difficult to understand for individuals with limited education. Formal language represents a
sort of academic language, most often found in a written form that many people neither use
nor completely understand. A permanent effort is required to make test instructions and, in
general, test language understandable for less educated people and appropriate for
different cultural and subcultural groups.
Education
Education plays a double role in test performance: school, on one hand, provides some
contents frequently included in cognitive tests; and school, on the other hand, trains some
learning strategies and develops positive attitudes towards intellectual matters and
intellectual testing. In consequence, school could be considered as a subculture into itself.
Greenfield (1997) has emphasized that A major (probably the major) factor that makes a
culture more or less different from the cultural conventions surrounding ability testing is the
degree of formal education possessed by the participants (p. 1119).
Learning to read reinforces certain fundamental abilities, such as verbal memory,
phonological awareness, and visuospatial discrimination (Ardila, Ostrosky & Mendoza,
2000; Ardila et al., 2010). It is not surprising that illiterate people underscore in cognitive
tests tapping these abilities. Furthermore, attending school also reinforces certain attitudes
and values that may speed the learning process, such as the attitude that memorizing
information is important, knowledge is highly valuable, learning is a stepwise process
moving from the simpler to more complex, etc. It has been emphasized that schooling
improves an individuals ability to explain the basis of performance on cognitive tasks
(Laboratory of Comparative Human Cognition, 1983). The fundamental aims of schools are
equivalent for all schools and school reinforces certain specific values regardless of where
they are located. Hence, school could be seen as a culture unto itself, a transnational
culture, the culture of school. School not only teaches, but also helps in developing certain
strategies and attitudes that will be useful for future new learnings. Ciborowski (1979)
observed that schooled and non schooled children can learn a new rule equally well, but
once acquired, schooled children tend to apply it more frequently in subsequent similar
cases.
Interestingly, education is not related with the ability to solve everyday problems.
Cornelious and Caspi (1987) found that educational level has a substantial relationship with
performance on verbal meaning tests but was not systematically related to everyday
problem solving (i.e., functional criterion of intelligence). Craik, Byrd, and Swason (1987)
observed that differences in memory loss during aging are related to socioeconomic status.
Ardila and Rosselli (1989) reported that during normal aging the educational variable was
even more influential on neuropsychological performance than the age variable. Albert and
Heaton (1988) argue that, when education is controlled, there is no longer evidence of an
age-related decline in verbal intelligence.
A significantly decreased neuropsychological test performance has been
documented in illiterate individuals (Ardila, 2000; Ardila et al., 1989, 2010; Goldblum &
Matute, 1986; Lecours et al. 1987a, 1987b, 1988; Manly et al., 1999; Matute et al., 2000;
Ostrosky et al., 1998; Reis & Castro-Caldas, 1997; Reis, Guerreiro & Petersson, 2003).
Rosselli, et al., 1990). Lower scores are observed in most cognitive domains, including,
naming, verbal fluency, verbal memory, visuoperceptual abilities, conceptual functions, and
numerical abilities. Language repetition can be normal for meaningful words, but abnormal
for pseudowords (Reis & Castro-Caldas, 1997; Rosselli et al., 1990). Similarly, copying
meaningful figures can be easier than copying nonsense figures (Ostrosky et al., 1998).
Furthermore, for illiterate people to use concrete situations can be notoriously easier than
using non-real and abstract elements. When the information is related to real life, it can be
significantly easier to understand. Thus, for the illiterate person, it is easier to solve the
arithmetical operation If you go to the market and initially buy 12 tomatoes and place them
in a bag and later on, you decide to buy 15 additional tomatoes, how many tomatoes will
you have in your bag? than the operation: How much is 12 plus 15? Semantic verbal
fluency is easier than phonological verbal fluency (Reis & Castro-Caldas, 1997; Rosselli et
al., 1990), seemingly because phonological abstraction is extremely difficult for the illiterate
person. Semantic verbal fluency requires the use of concrete elements (animals, fruits)
whereas phonological fluency is tapping a metalinguistic ability. The very low scores
observed in neuropsychological tests in illiterates can be partially due to differences in
learning opportunities of those abilities that the examiner considers most relevant, although,
they are not the really relevant abilities for illiterates' survival. They can be also due to the
fact that illiterates are not used to being tested. Furthermore, testing itself represents a
nonsense situation that illiterate people may find surprising and absurd. This lack of
familiarity with a testing situation represents a confounding variable when testing individuals
with limited education.
Several studies have demonstrated a strong association between educational level
and performance on various neuropsychological measures (e.g., Ardila, Rosselli &
Ostrosky, 1992; Bornstein & Suga, 1988; Finlayson, Johnson & Reitan, 1977; Heaton,
Grant & Mathews, 1986; Leckliter & Matarazzo, 1989; Ostrosky et al., 1985, 1986).
However, some tests are notoriously more sensitive to educational variables (e.g.,
language understanding tests) than others (e.g., orientation tests). Extremely low scores in
current neuropsychological tests are observed in illiterate people (e.g., Ardila, Rosselli &
Rosas, 1989; Rosselli, Ardila & Rosas, 1990). Low scores in neuropsychological tests
observed in illiterates can be partially due not only to differences in learning opportunities of
those abilities that the examiner considers relevant (although, evidently, they are not the
really relevant abilities for illiterates' survival) and to the fact that illiterates are not used to
being tested (i.e., they have not learned how to behave in a testing situation), but also, that
testing itself represents a nonsense (non-relevant) situation (Ardila, 1995).
This educational effect, nonetheless, is not a linear effect, but rather it is a negatively
accelerated curve, ending in a plateau. Differences between zero and three years of
education are highly significant; differences between three and six years of education are
lower; between six and nine are even lower; and so forth. And virtually no differences are
expected to be found between, for example, 12 and 15 years of education. The reason is
simple: the ceiling in neuropsychological tests is usually low (Ardila, 1998). Table 8.1
presents the differences in some cognitive tests between illiterates and subjects with onetwo and three-four years of education and Figure 8.1 illustrates a specific example.
_______________________________________________________________________________
Years of education
Test
1-2
3-4
_________________________________________________________________
Digits backwards
2.4
2.6
2.7
Verbal memory
4.2
4.2
4.3
Copy of a figure
7.5
8.8
9.4
Naming
7.3
7.3
7.5
Comprehension
3.7
4.4
4.6
Semantic fluency
13.5
14.6
15.4
3.3
6.5
7.0
Phonologic fluency
________________________________________________________________________________
Note: mean scores are presented
Table 8.1. Effect of education on test performance in some selected subtests of the
NEUROPSI neuropsychological test battery (n=807) (adapted from Ostrosky et al.,
1999).
Figure 8.1. The educational effect is not a linear effect, but rather it is a negatively
accelerated curve, ending in a plateau. Example of the Copy of a Semi-Complex
Figure test (adapted from Ostrosky et al., 1999).
Although it is well established that there a significant correlation between cognitive

test scores (e.g., IQ) and school attendance (e.g., Matarazzo, 1972) interpreting this
correlation has been polemic (Brody, 1992; Finch et al., 2011; Neisser et al., 1996). The
really crucial question is: Do cognitive (intelligence) tests indeed predict school
performance? Or rather, does school train those abilities appraised in intelligence tests? To
answer these questions is not easy, even though frequently the interpretation has been that
IQ predicts school performance (e.g., Hunter, 1986). Other researchers, however, consider
that IQ scores are to a significant extent a measure of direct and indirect school learning
(e.g., Ardila, 1999; Ceci, 1990, 1991).
Ceci and Williams (1997) presented an impressive and detailed review of the
available data in this area. Seven types of historical evidence for the effect of schooling on
IQ were examined:
(1) The effect of intermittent school attendance: several studies have provided
converging evidence that the longer youngsters stay out of school, the lower their IQs.
(2) The effect of delayed school start-up. Different studies have demonstrated
that children whose schooling was delayed experienced a decrement in several IQ points
for every year that their schooling was delayed.
(3) The effect of remaining in school longer. As a result of extra schooling (to
avoid military service), men born on a particular date (July 9 instead of July 7) earned
approximately a 7% rate of return on their extra years of schooling. The authors point out
that this figure of 7% is very close to the estimate of the return on an extra year of
schooling derived from studies of being born early or late in a given year.
(4) The effect of discontinued schooling. There is a well-established detrimental
effect of dropping out of school before graduating. For each year of high school not
completed, a loss of 1.8 IQ points has been observed.
(5) The summer school vacations. A systematic decline in IQ scores occurs during
summer months. With each passing month away from school, children lose ground from
their end-of-year scores on both intellectual and academic scores.
(6) The effect of early-year birth dates. Given the age limits to enter school in the
US, within a given year, the number of years of schooling completed is the same for those
born during the first nine months of the year. But the amount of school attendance drops off
for those born during the final three months of the year. After coming of age, some
individuals leave school, and students with late-year births are more likely to stay in school
one year less than students with early-year births. It has been observed that for each year
of schooling that is completed there is an IQ gain of approximately 3.5 points.
(7) Cross-sequential trends. A correlation between the length of schooling

completed and intellectual performance among same-age, same-SES children has been
observed.
The general conclusion is that school attendance accounts not only for a substantial
portion of variance in children's IQ but also apparently some, though not all, of the cognitive
processes that underpin successful performance in IQ tests. The magnitude of this
influence ranges between 0.25 to 6 IQ points per year of school (Ceci, 1991). In
consequence, the association between IQ and education cannot be interpreted assuming
that IQ predicts school success. Intelligence and schooling have complex bi-directional
relationships, each one influencing variations in the other (Ceci & Williams, 1997).
According to our results (e.g., Ardila et al., 2000b) even though bi-directional
relationships between intellectual test performance and schooling may exist, the really
significant relationship is between schooling and cognitive test performance. That is,
attending school significantly impacts cognitive test performance.
Culture minorities groups

Cognitive testing of so-called minority groups represents a special situation in
neuropsychology assessment. Minority groups constitute a culture or subculture within a
mainstream culture. Quite often, the tester belongs to the majority culture and may have a
limited understanding of the minority culture or subculture. Testing is likely interpreted from
the majority culture perspective. To be a member of a minority group, however, has
significant implications that can affect the testing situation and the testing results.
There are over 120 million people living in a country different from that one where they
were born. They are "minorities in the new host country: Turkishes in Germany,
Moroccans in Spain, Hindus in England, Colombians in Venezuela, Greeks in Switzerland,
Rwandans in Zaire, Mexicans in US, Greeks in France, etc. There are also some ethnic
groups that are minorities in their own countries: African-Americans in US, Kurds in
Turkey, Ameridians in Colombia (and virtually in every country), etc. Finally, there are some
groups that are minorities everywhere because they do no have a country. Currently
Gypsies are the best example, but until recently, Jews were also a peoplehood without a
country.
To be different from the mainstream people has a significant psychological impact.
Patterns of behavior, beliefs, and attitudes may be different. Language can impair normal
communication with the majority group. Even physical appearance and dressing can
separate and distinguish the minority people. In the US there are hundreds of groups that
can be regarded as minorities.
At least six different variables can potentially distinguish the minorities groups. They
may also affect intellectual test performance and the psychology of minority:
1. Nationality:
is that person regarded or not as an alien? Intermediate
possibilities can exist. For instance, Hispanics in the US have five different
possibilities: US born (2 possibilities: from the mainland or from Puerto Rico),
acquired citizenship, legal immigrant, and illegal immigrant. It makes a significant
difference if the country where you are living in is legally your country or you are
a non invited alien.
2. Culture (relative distance). Irish immigrants in US have a closer culture to
mainstream American way of life than Ethiopians. The larger the cultural
distance, the more separated you are to understand the new culture and
appropriately behave in it.
3. Language (relative distance). Minorities may speak a different language, may

speak a dialect of the majority language, or may simply speak the same
language. The ability to communicate, and hence, participate (e.g., to have a
job) in the host culture highly depends on the ability to speak. Language distance
between English and German is lower than language distance between English
and Spanish. Language distance between English and Chinese is huge. Age
also plays a crucial role in the ability to learn the new language. Young Moroccan
people in Spain can easily learn Spanish and improve in social status, whereas
adults have to accept low qualified and paid jobs.
4. Normality (how frequent -- normal-- is your group in your living environment). To
be different depends on the community you live in. Hispanics are the normal
people in Miami, but very unusual people in Fargo. To be unusual may be
associated with suspiciousness in the majority group and paranoia in the minority
people.
5. Reference group (How many people are like you are). It depends upon with
what specific group is the identification. Hispanics for instance, can consider that
their reference group is Latin America or other US Hispanics. In the fist case the
reference group is even larger than the majority US group. In the second one it
is a notoriously smaller and weak social reference group. Finally,
6. Social image: Positive or negative attitudes in the majority group toward the
minority people. Even though minorities have in general a low social image (e.g.,
they are poor, with low education, inappropriate behaviors, etc.) some times
positive attitudes are also associated with the minority group. For instance,
Oriental people are frequently regarded in the US as intelligent and hardworking people.
Neuropsychological testing of minority groups have progressively become a more
and more important question in neuropsychology, particularly in some countries with a
significant immigration flow (e.g., some European countries). It is not easy for a Spanish
neuropsychologist to test a Moroccan patient, or for a Danish neuropsychologist to test a
Somalian client. There are not obvious answers to questions such as, how to carry the
testing, what specific tests to use, and what conclusions can potentially be drawn from the
testing results.
Norms in different national and cultural groups

A tremendous effort has been devoted in neuropsychology to obtaining test performance
norms (e.g., Ardila et al.., 1994; Lezak, 2004; Spreen & Straus, 1998). Currently, many
neuropsychological tests possess relatively solid and reliable norms. Nonetheless, norms
have been obtained in most cases in white English-speaking, middle-class subjects with a
high-school or college level of education.
In cognitive testing it is usually assumed that norms are always required. Otherwise, no
comparison is reliable. This idea, however, is more a desideratum than a reality. Furthermore,
it does not seem to be a completely realistic idea. As a matter of fact, in the future, the search
for norms may be coordinated with the search for understanding the sources of variation. Two
evident problems with norms are readily observed:
1. Language. To obtain norms in English or Spanish (each one with about 400 million
speakers) seems realistic. But English and Spanish are just two out of the three
largest existing languages accounting together for no more than 15% of the worlds
population.
Worldwide,
there
are
about
6,800
different
languages
(http://www.ethnologue.com/), most of them, with a limited number of speakers. As

an example, in Mexico 288 Amerindian languages are currently spoken
(http://www.ethnologue.com/). In the USA, over 300 languages are found, when
counting both Amerindian and immigrant languages (http://www.ethnologue.com/).
To obtain norms for all these 6,800 different languages is simply unrealistic.
Furthermore, most of the world languages are small languages, and obtaining a
reliable database would mean testing a high percentage of the speakers. If we
assume that the average language has one million speakers (the real number is
lower), and we want to normalize the neuropsychological instruments using just 200
stratified subjects in each language, it would mean that about one and half million
participants would be required. This is a nonrealistic endeavor for contemporary
neuropsychology.
It seems more realistic to determine the linguistic factors
potentially affecting cognitive test performance. A diversity of languages could be

selected, comparison established, and significant variables distinguished. Language
idiosyncrasies seem most important in understanding potential sources of variations.
Obtaining norms is a realistic endeavor in English, Spanish, Quechua or Bengali, but
does not seem realistic for the 288 Amerindian languages spoken in Mexico.
2. Culture. There are solid bases to assume significant cultural variations in
psychological and neuropsychological test performance (e.g., Ardila, 1995;
Fletcher-Janzen et al., 2000; Nell, 2000; Uzzell et al., 2007). Thus, the question
becomes, how many cultural groups should be separated? Although several
thousand different cultures have been described by anthropology (e.g., Bernatzik,
1957), obviously, there is not a definitive answer to this question. Cultures frequently
represent a continuum, and cultures can partially overlap. For example, if asked
whether separate norms should be used when testing Caucasians and Hispanics in
the US, most neuropsychologists might answer YES. Nonetheless, a diversity of
conditions may separate Caucasians and Hispanics: primary language (for many
Hispanics, their primary language is English; most Hispanics are bilinguals, some
are monolingual; the degree of mastery of Spanish and English is tremendously
variable), acculturation (degree of assimilation of the modal American culture
values is highly variable), etc. So, there does not seem to be an obvious and direct
answer. To be Hispanic or Caucasian is not a dichotomy. Another question: In
the US, can the norms obtained in San Francisco be used to test people in Boston,
San Antonio, Honolulu, or Anchorage? San Francisco is a quite heterogeneous city
and the question becomes what specific San Francisco norms are going to be used
with what specific population in Boston, San Antonio, Honolulu or Anchorage? The
same type of question can be raised everywhere. For instance, can we use the
norms obtained in Barcelona, Spain to test people in the Canary Islands, Santiago
de Compostela or Bilbao? The answer in all these cases may be, partially yes,
partially no. This is indeed an endless question. If we move to the worldwide
situation (with thousands of cultural variations!), we may conclude that this is also a
nonrealistic endeavor for psychology and neuropsychology. I am proposing that this
question has to be re-stated, and instead of looking for norms in every existing
human group, we should try to understand why culture may impact and how culture
impacts cognitive testing, i.e., which are the specific cultural variables that may
affect the performance in a psychological or neuropsychological tests (Ardila, in
press). For this purpose, it seems more reasonable to select a series of rather
different cultural groups, representing enough cultural dispersion, in an attempt to
pinpoint those cultural variables potentially affecting cognitive test performance.
In brief, understanding the variables that can affect cognitive test performance seems to
be as important as obtaining a large number of norms in different linguistic and cultural
groups. (Ardila, Ostrosky & Bernal, 2006).
For example, there does not seem to exist any reason to find differences in verbal
fluency in pre-school and school children when using an equivalent semantic category in
Spanish and English. If the familiarity with the testing condition is equivalent (both are small
children with little or no familiarity with testing), the level of education is the same (none or
whatever), the age is the same, and the semantic category has the very same semantic
field in both languages, no differences in performance are expected. Table 8.2 presents
the norms obtained by Halperin et al. (1989) in the US and Ardila and Rosselli (1994) in
Colombia. Even though the age groups were divided differently (Halperin et al. used one
year range; Ardila & Rosselli used two-year range) it is evident that performance was
virtually identical.
__________________________________________________________________
Halperin et al., 1989
Ardila and Rosselli, 1994
(USA)
(Colombia)
__________________________________________________________________
Age
(years)
Age
n
SD
(years)
SD
__________________________________________________________________
6
34
10.74
2.40
40
12.43
2.90
32
12.31
2.70
38
13.76
3.70
10
22
14.27
3.70
11
28
15.50
3.80
12
10
18.90
6.20
5-6
49
9.33
3.65
7-8
63
11.49
2.87
9-10
56
14.09
3.99
11-12
65
16.75
4.64
__________________________________________________________________
Table 8.2. Semantic verbal fluency (ANIMALS) in US and Colombia.
Table 8.3. compares performance in two verbal fluency tests (phonological and
semantic verbal fluency) in Spanish and English monolingual speakers. As anticipated,
performance is virtually identical, if confounding variables are controlled. English speakers
do a little better when using some letters; Spanish speakers do a little better when using
other letters, very likely depending upon the frequency of words beginning with that
particular letter in each language, the potential ambiguity existing between homophone
letters, and some other uncontrolled confounding variables. Performance in semantic
verbal fluency using the category ANIMALS was virtually identical.
____________________________________________________________________
English
Spanish
____________________________________________________________________
F
12.9 (5.4)
11.7 (4.1)
10.7 (5.1)
11.8 (4.6)
13.8 (5.4)
11.4 (3.8)
Animals
16.8 (5.2)
16.7 (3.8)
Note. Mean scores and standard deviations are presented.
Table 8.3. Semantic verbal fluency (ANIMALS) in Spanish and English monolinguals
(60-65 years; 13-16 years of education (according to Rosselli et al., 2000).
Nonetheless, unexpected confounding variables can exit. Digit span looks like a
relatively culture-fair test, and similar performance might be anticipated in people from
different human groups. Nonetheless, that is not the case. A significant variability has been
observed. Digit span varies from 5.4 (Poland) to 9.0 (China) (Dehaene, 1997; Nell,
2000).The reason for this variability is not totally clear, but both linguistic and training
factors seem to exist (Dehaene, 1997). The phonological length of digits (number of
phonemes included in digit words) as well as previous exposure to similar tasks (e.g., to
say phone numbers using digit-by-digit strategy) may play a significant role in digit span. In
the Sikuani language spoken in the Amazon jungle digits are: kae (one) , aniha-behe (two),
akueyabi (three), penayanatsi (four), kae-kabe (five), kae-kabe kae-kabesito-nua (six),
kae-kabe aniha-kabesito-behe (seven), kae-kabe aniha-kabesito-akueyabi (eight),
kae-kabe aniha-kabesito-penayatsi (nine). With such long words, it can be conjectured that
digit span will be very low.
What is proposed is that understanding the variables potentially affecting (and
confounding) test performance may be as important as obtaining norms for different human
groups.
No doubt, understanding cultural variables in cognition represents a major research
area during the twenty-first century.
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ON THE ORIGINS OF HUMAN COGNITION

Statement of the Problem

There are only two fundamental aphasia syndromes

The selection disorder

The sequencing disorder

Other aphasia syndromes

Three stages in language development

Initial communication systems

The function of noises (grunts) in human communication

Second stage: Lexical/semantic

Third stage: Grammar

Brain representation of nouns and verbs

Memory systems for nouns and verbs

Using verbs and using grammar is a single ability

Understanding Brocas area

Origins of the lexical/semantic system

Origins of the grammatical system

Grammar at the origin of the executive functions

3. Origins of Spatial Abilities

How we get oriented in the space?

Cultural Differences in Visuoperceptual Abilities

Acquired spatial cognition disorders

How did writing appear?

How many people can write?

Agraphia as a neuropsychological syndrome

Is any area in the brain specialized for writing?

Brain activation during writing

Writing in different systems

From agraphia to dystypia

5. Origins of Calculation Abilities

Numerical concepts in animals

Development of calculation abilities in children

Numerical abilities in pre-school children

Development of numerical abilities at school

Calculation abilities in pre-historic man

Further developments of arithmetical abilities

The neuroscience of calculation abilities

6. Origins of Executive Functions

What does executive functions mean?

Is there any fundamental core ability accounting for

Two proposed fundamental executive functions

Metacognitive executive functions as an internalization

Executive functions in pre-historical man

Metacognitive executive functions as a cultural product

7. How we recognize other people?

Own-species members recognition

Emotional expression and emotional recognition

8. Culture and Cognitive Testing

Why culture affects cognitive test performance?

Culture minorities groups

Norms in different national and cultural groups

Statement of the Problem

On the Origins of Human Cognition 10

pictorial rests (Spennemann, 1984).

On the Origins of Human Cognition 11

On the Origins of Human Cognition 12

1. To integrate some information regarding cross-cultural differences in

On the Origins of Human Cognition 13

In the chapter Origins of Writing it is argued that there is no brain area

On the Origins of Human Cognition 14

On the Origins of Human Cognition 15

cognitive test performance? is approached. Different cultural aspects potentially affecting

On the Origins of Human Cognition 16