Cochlear mechanics,nonlinearities,and cochlear

potentials
Peter Dallos, Mary Ann Cheatham, and John Ferraro
Auditory ResearchLaboratory,Departmentof ElectricalEngineering,* NorthwesternUniversity,Evanston,
Illinois

60201

Cochlearmicrophonic(CM) magnitudefunctionsare shownfrom variousturns of the cochleaat

constantsoundpressurelevel (SPL), constantstapesdisplacement,and constantstapesvelocity.The
similaritiesof thesecurveswith basilar membranedisplacementfunctionsare considered.The
influenceof CM nonlinearityon the shapeof the plots is discussed,and it is demonstratedthat the
responseis extremelynonlinearin a narrow frequencyrange abovethe best frequencyof the
electrodelocation,while at other frequenciesit is much more linear. All nonlinearphenomenathat
are demonstrablein cochlearpotentials,namely harmonicdistortion,summatingpotentialgeneration,
and interferenceeffect, are primarily concentratedin the aforementionednonlinear frequencyregion.
SubjectClassification:65.26, 65.40.

CM to preceding mechanical events (Dallos et at., 1972b;

INTRODUCTION

The cochlear microphonic potential (CM) is one of the

most thoroughly investigated, one of the potentially most
useful, and one of the most misunderstoodand misrepresented biological phenomena that is associated with the
functioning of the ear.
Some assume that the CM acts
as a direct stimulus to the dendrites of the auditory

nerve, while others consider it a mere epiphenomenon.

Several papers have appeared recently indicating a degree of correlation between various aspects of CM and
other auditory phenomena, such as behavioral threshold
(Price, 1971), single unit response characteristics in
the 8th nerve (Pfeiffer and Molnar, 1970), and two-tone
suppression (Legouix et at., 1973). Yet there are other
publications showing a decided lack of correlation between CM and other indices of the functioning of the auditory system, or advising caution in the interpretation of

CM data (Whitfield and Ross, 1965; Weiss et at., 1971;

Dallos, 1969b; Dallos et at., 1971). There are two major factors that make the interpretation

of CM data diffi-

cult, and the development of one-to-one relationships between CM and the motion of one point of the basilar membrane, or CM and the response of a single auditory
nerve

fiber

hazardous.

These

two factors

are

the com-

plex relationship between the recorded gross CM and the

outputs of individual hair cells, and the more, or less,
nonlinear

behavior

neural events.

of the CM than either

mechanical

or

The previous problem has received con-

siderable attention during the past several years (Whitfield and Ross, 1965; Weiss et at., 1971; Dallos et at.,

1971;Kohll'ffel, 1971; Laszloet at.

1972; Haas,

1973). It is thus suggested that only under particular

limited conditions does the gross CM provide an adequate representation of the electrical output from the
hair cells in the immediate vicinity of the recording
electrodes.
Generally the gross CM is the vectorial
sum of the potentials generated by literally thousands
of cells, each excited at a different amplitude and phase,
and each. seen through the complex electrical network of
the electrolyte-filled

membraneous cochlea.

It has also

been shown, however, that when appropriate recording

techniques are used and proper caution in interpretation
is exercised, then valuable inferences can be drawn from

597

J.Acoust.
Soc.Am.,Vol.55,No.3, March1974

Dallos, 1973). These correlations between mechanical

and hydrodynamic phenomena and CM are further examined in this paper. We are also addressing ourselves
to the much neglected problem of how the nonlinearity of
the CM itself can distort the relationship between the recorded potential and its mechanical precursor.
I.

METHOD

All data reported in this paper were obtained from

anesthetized guinea pigs whose tensor tympani tendons
were cauterized.
The electrical potentials, CM and
summating potential (SP), were derived from differential electrode pairs placed in various turns of the
cochlea. The sound pressure was accurately monitored
at the eardrum with a probe tube microphone.
All CM
data were measured with a 3 Hz bandwidth wave analyzer,
while all SP data were obtained from averaged records
from

which

the CM was

eliminated.

The

details

of ani-

mal preparation and various recording techniques have

been described by us in several publications (Dallos,

1969a; Dallos et at., 1969; Dallos et at., 1972a).

Much of the data presented in this communication are
in the form of potential magnitude versus frequency
functions with various input quantities held as constant
parameters. Three such input quantities are considered:
sound pressure level at the eardrum, stapes displacement, and stapes velocity. The first of these has the
advantage of ease of measurement, but of course the
resulting cochlear potential functions incorporate significant middle-ear effects with the consequence that
it is somewhat difficult to interpret the results in terms
of cochlear mechanics. When stapes displacement is
held

constant

then

middle

ear

influences

are

eliminated

and the resulting functions are most directly comparable

with data in the literature pertaining to basilar mem-

brane displacement(Bksy, 1960; Johnstoneand Boyle,

1967; Rhode, 1971; Wilson and Johnstone, 1972). Finally, when stapes velocity is the constant parameter,
once again the middle ear effects are removed, and the
theoretically most appropriate choice of cochlear input
variable is employed.
This is the case because the el-

Copyright
1974bytheAcoustical
Society
of America

597

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598

Dallas, Cheatham, and Ferraro: Cochlear mechanicsand potentials

598

Middle

fective input to the cochlea is pressure at the oval window, and this pressure is proportional to the product of
stapes velocity and cochlear input impedance. In the
guinea pig the acoustic input impedance of the cochlea
is resistive and constant at all significant audio frequen-

transfer

SPL

ear

function

correction

SPL

for constant stopes

correction

for constant stapes

velocity

displacement
SPL

SPL

cies (Dallos, 1970) consequently stapes velocity is di-

rectly proportional to pressure at the oval window--the

input quantity of choice.
Since it is impractical to measure stapes velocity or
displacement during every experiment, one needs to
rely on available middle ear transfer functions to infer
these quantities from the measured sound pressure at
the eardrum.
We have been employing two methods of
correcting for middle ear characteristics.
In one
method, families of CM versus frequency functions are
obtained for constant sound pressure in 10 dB steps be-

400

400

400

frequency (Hz)

FIG. 1.

(a) Schematic of middle-ear transfer function: stapes

displacement as a function of frequency at a constant sound

pressure at the eardrum.
(b) Correction factors for SPL in
order to keep stapes displacement constant. (c) Correction
factors for SPL in order to keep stapes velocity constant.

tween20 and100dB(re O.0002dyn/cm'). From these

functions the desired constant stapes displacement or
constant stapes velocity plots are obtained by interpolation on the basis of an average middle ear transfer function. In the other method the sound pressure level of

the stimulus is changed from frequency to frequency,

again on the basis of an average middle ear transfer
function, so as to produce constant stapes displacement
or velocity.
Since the middle ear is linear well beyond
the intensity range that we utilize, the two methods are
expected to yield identical results, and indeed they
demonstrably
There

are

do.
two sets of available

of guinea pig middle ear transfer

direct

measurements

functions in the litera-

ture. These functions (Johnstoneand Taylor, 1971;

Wilson and Johnstone, 1972) apply to the open bulla
condition which is utilized in all our experiments and
they are highly similar.
Considering that the two functions are derived on the basis of different experimental
techniques (M6ssbauer method versus capacitive probe

measurement) their similarity is encouraging and warrants

their

use.

The

main

characteristic

of both of

these functions is that when sound pressure is held constant at the eardrum the stapes displacement remains
constant up to about 400 Hz, beyond which it decreases

at an approximate
rate of 8-9 riB/octave.
Thereare
some resonant peaks superimposed on this general pattern, but presumably the magnitude and frequency of
such peaks is highly variable from animal to animal

(Guinanand Peake, 1967) and thus their incorporation

into an "average" correction curve is unwarranted. In
Fig. 1 a schematic representation of the middle ear
transfer function is given together with correction plots
derived from it for obtaining the constant stapes displacement or constant stapes velocity data. Accordingly, if one wishes to hold stapes displacement constant
then the sound pressure level should be maintained at a
constant value up to 400 Hz, beyond which it should be

increased at a rate of 8 riB/octave. Whenconstantstapes

stapes motion at 100 dB SPL at the drum is of the order

of 0.3 z, or usinglinear extrapolationit is 1 / at 30

dB SPL. Where appropriate we will use this value and
designate constant stapes displacement curves in terms

of dB re 1 .
II.

RESULTS

AND

DISCUSSION

Von Bksy's (1960, pp. 680-682) classic experiments utilizing the vibrating electrode provided the first
direct indication of the relationship between basilar
membrane motion and cochlear potentials.
He demonstrated that a trapezoidal displacement of the cochlear
partition produced a trapezoid-shaped microphonic response. The conclusion that can be drawn from these
experiments, now widely accepted as one of the .funda-

mental relations in cochlear physiology, is that the CM

is proportional to the displacement of the cochlear partition. Some of our recent work has provided an amendment to the above statement.

It is our contention that

the CM produced by the outer hair cells is proportional

to the displacement of the cochlear partition, but that
the inner hair cell--produced CM is proportional to the

velocity of the partition (Dallos et al.,

1972b; Dallos,

1973). This modified description of the functional relation between microphonic time patterns and basilar

membrane motion merely extends yon Bksy's observations and is in no way in conflict with them. To
explain, consider that the electrical output of the outer
hair cells is considerably in excess of what is generated
by the inner hair cells. This has been demonstrated by

Davis et al. (1958) and to some extent quantified by us

(Wang, 1971; Wangand Dallos, 1972; Dallos and Wang,

1974). An example indicatingthe differences involved
in CM production by the two hair cell groups is shown
in Fig. 2. Included in the figure are CM input-output
functions for one kanamycin-treated guinea pig and the

median function (along with interquartile range) obtained

from a group of normal animals. These functions repre-

velocity plots are sought then the input sound level is de-

sent the CM response recorded from the first turn of the

creased at a rate of 6 riB/octave up to 400 Hz and increased at a rate of 2 riB/octave above this corner fre-

cochlea with a continuous

quency.

trode technique, consequentlyremote CM is largely

One can glean from the data of both groups of investigators that at low frequencies the rms amplitude of

rejected. The insert in the figure shows the cochleogram of the abnormal animal whose CM function is presented. This plot demonstrates that in the neighbor-

8000-Hz

tone as the stimulus.

The recording is performed with the differential

elec-

J. Acoust.Sac.Am., Vol. 55, No. 3, March1974

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599

Dallas,Cheatham,
andFerraro:
Cochlear
mechanics
andpotentials

i
100i--::.-.-.-.-.-.-.-.-.-
,,-;,-,-':-':.
-

! i
.

i i

i i

1973).

i
- 5

OHC

zo

I0

so

15

DISTANCE
FROMAPEX
1

,20

4th 3rdI 2ridI

f =8000Hz
2

SPL

E[G. 2.

Input-output [unctons [o C

ioo

placed in the first turn of the cochlea. The graphs show

CM magnitude as the function of stimulus frequency at
50 dB SPL, at the corresponding (at low frequencies)

12o

(dB)

at 8000 Hz :eco:ded

[:om the fi:st turn of the cochlea. Heavy filled c:cles :ep:esent data [:om one andrea[whose coch[ea ws poisoned by
Eanamycn njecHons. The coch[eog:am of ths andrea[ s
shown n the nse:t. ote that n the vcty of the :eco:dng
e[ect:ode pa: (a::ow) on[y nne: ha[: ceUs ([HC) a:e p:esent.
The nput-output [uncton :ep:esented by [gh[ symbols s a
median no:m[ p[ot (a[ongwth nte:qua:t[e :ae).

hood of the recording electrodes (arrow) the cochlea is

completely denudedof outer hair cells, while over 95%
of the inner hair cells are present.
assumption that in this case the CM
ferential electrode pair is produced
cells near the electrodes.
We may
outer

hair

cells

are

about

It is a reasonable
recorded by the difby the inner hair
conclude that the

30 dB more

sensitive

than the

innerones,1andthat, at anyintensitylevel the outer

hair cells produce considerably more CM than their inner counterparts.
The latter conclusion is apparent

when one notes that the kanamycin animal's CM function

(inner hair cells only) peaks at about the same place,
but always lies below, the function of the normal population (both inner and outer hair cells). Several results
follow from these observations.
First, and most important, is the necessary conclusion that in a normal
animal the recorded CM can be construed as being determined almost exclusively by the outer hair cell population.
This is the case since at any level the contribution of the inner hair cells to the total response is at
most

one-tenth

of the

contribution

of the outer

hair

also be seen from

stapesdisplacement
of 10 ., andat the approximate
stapesvelocityof 25000,/sec. Whensoundpressure
is kept constant, the CM magnitude rises at an approxi-

mate rate of 6 dB/octaveupto about400 Hz, beyond

which it declines in an irregular fashion until it reaches
a frequency where a variable size peak occurs. Beyond
this peak the response drops rapidly (approximately

20-40 dB/octave)with further increase in frequency.

In many animals there is a strong indication that after
the response magnitude declines about 20 dB, it levels
off at that value for higher frequency stimuli. We are
uncertain whether this high-frequency plateau is a real
physiological phenomenon or a manifestation of unre-

jected remote response (Dallos et al., 1971). Between

400 Hz and the aforementioned peak the overall rate of
decline of the response is about 8-9 dB/octave. The
position of the response peak that occurs just prior
to the eventual decline of the CM at high frequencies
is the most characteristic quantity that distinguishes
the responses obtained from different

cations.
300

that

lo-

coMtant

stapes

displacement

I00

"'30-

:o -

schemes would necessitate that the CM phase difference

stapes

velocity
TI

t,

o.,

o.s

Frequency

such cancellation

produced by the two cell groups be between 120 and

180, whereas our experiments demonstrate that the
phase difference between inner and outer hair cell generated CM is 90 or less (Dallos et al., 1972b; Dallos,

constant

3-

1972) are not tenable. This can

the contrast

electrode

When the frequency where the response

cells.

Thus the CM generated by the inner hair cells has negligible influence on the total, normal, response. We can
thus say, in harmony with yon B&k&sy, that in a normal
cochlea (dominated by outer hair cells) the CM is proportional with basilar membrane displacement.
Another
conclusion that can be drawn from the plots of Fig. 2 is
that schemes that attempt to explain the declining segment of the CM input-output function by postulating a
cancellation between the CMs produced by the two cell

groups (Karlan e! l.,

In the present paper our concern is with the electrical

response of the normal cochlea, and it is now understood on the basis of the above arguments that such a
response reflects the aggregate electrical output of the
outer hair cells. It is now appropriate to begin our discussion of the relationships between cochlear potentials
and mechanical events by comparing the CM functions
generated by the three previously discussed methods:
constant SPL, constant stapes displacement, and constant stapes velocity. To aid the comparison in Fig. 3
a set of plots is presented as obtained from electrodes

20 I 0 I 6 I 8 I

599

FIG. 3.

constant

SPL

,o

(kHz)

CM: magnitudes obtained rom the first turn oone

nea pig at constant50-dB soundpressure level, andor

SPLs adjusted according to the plots of Fig. 2 to yield constant
stapes displacement or constant stapes velocity. In this case
the adjustments result in a constant stapes displacement of

10 andvelocityof 25000k/sec.

J. Acoust.Sac.Am., Vol. 55, No. 3, March1974

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600

Dallos,Cheatham,and Ferraro:Cochlearmechanics
andpotentials

Basilor

part. The reason for the discrepancy can be related to

at least two problems. First, the mechanical plot is
not obtained at a constant stapes displacement, instead
it is the ratio of basilar membrane and incus displacements. Assuming negligible differences between the
movements of the incus and the stapes, the two previous
measures can yield similar results only if the displace-

membrane

displacement

20

per incus displacement

io

ments

.--

"'

CM at constant

stapes
displacement
at 4.0

-2:0',
'
Ol

0.2

FIG.

4.

'

'

'

'

'

'

I0

20

50

Comparison

ear

structures

and basilar

mem-

(Rhode, 1971). Thus the method of data collection could

mm

0.5

Frequency

of both middle

brane are linear.

While the former linearity is reasonably well established, there are very serious doubts
about the linearity of the basilar membrane displacement, especially near its characteristic frequency

.-I0

600

conceivably yield a function with an exaggerated peak.

In contrast, the method Of recording CM almost certainly results in the flattening out of the resonant peak.
The intracochlear electrodes record potentials from

(kHz)

of CM magnitude obtained at constant

stapesdisplacement
(1 .) from one of our guineapigswith
basilar membrane displacement divided by incus displacement
as measured in a guinea pig by Wilson and Johnstone (1972).
In both experiments the point of measurement is approximately
the same. The ordinate is arbitrary logarithmic scale.

has dropped 3 dB from its peak value is obtained

from many animals, and when the median values
are plotted against distance of the recording electrode, then a straight line obtains in a semilogarithmic
coordinate system.
This cochlear map indicates that
the characteristic frequencies that belong to the usual

first, second, and third turn electrode locations (4, 10,

and 14 mm) are 12 000, 2200, and 750 Hz, respectively
(Dallos, 1973). When the plots are obtained with stapes

cells

distributed

over

a considerable

extent

of the inner-

ear spiral. Significant contribution can be expected

from cells located as far as 2 mm away from the elec-

trodes. Since the mechanical resonance is highly localized and since the electrical recording is not, it is
reasonable to expect that the latter should reflect a
spatial average and thus to result in a flatter function.
A similar argument can explain the discrepancy between
the high-frequency slopes of the CM and the basilar
membrane

functions.

Let us now return to Fig. 3 and consider the CM plot

that can be obtained when the input quantity of choice is
constant stapes velocity. This plot is reasonably
flat for all frequencies up to the resonance and the subsequent rapid decline in the response. As has been

stated (Weiss et al.,

1971; Dallos, 1973) the flatness

displacement held constant, they become directly com-

of the plot indicates that at any location in the cochlea

parable to data showing basilar membrane displacement

as a function of frequency.
The similarity between the
CM plots and the mechanical displacement plots is quite
compelling while the differences are revealing.
To
facilitate comparisons in Fig. 4 one of our constant
stapes displacement plots obtained from the first turn

the CM is proportional to stapes velocity up to a characteristic frequency.

A similar conclusion can be
reached from CM phase data as well. When referred
to the phase of the sound field at the eardrum the low-

(approximately 4 mm) is compared with one function

presented by Wilson and Johnstone (1972) for the ratio
of basilar
ticular

membrane

set

to incus displacement.

of mechanical

data

was

chosen

This parbecause

it is

the one reported where the measurement is obtained

closest to our customary electrode location.
The plot
shown is based on measurements at 4. I mm. The major
trends

tions

in both the CM

are

similar

and the mechanical

below

5000 and above

motion

18000

Hz.

func-

At

low frequencies both functions rise gradually, while at

the highest frequencies

they both flatten out.

The major

peak occurs in the same region in both plots, but the

height of the peaks is strikingly different.
Above 5000
Hz the basilar membrane displacement undergoes a

rapid increase, this "resonance"is apparentin most

contemporary measurements (Rhode, 1971; Johnstone
and Taylor, 1970). The size of the resonant increase

frequency CM phase is a 90 lead, while when referred

to stapes velocity, there is no phase shift at low frequencies. Another instructive means of relating CM
patterns to stapes displacement is by using very simple
temporal patterns in setting the latter in motion. For
example, if the stapes can be moved with a triangular
time pattern, and if the CM does indeed reflect the
velocity of the stapes, then it is expected that at any
point in the cochlea the recording electrodes would pick
up a square-wave CM pattern. We have demonstrated

(Dallos and Durrant, 1972) that this expectation is largely borne out. It was shown that with a triangular time
pattern of stapes displacement the electrical response
clearly approximates a square-wave, indicating the
fundamental validity of the assumption that CM is proportional to stapes velocity.
An interesting observation
was the approximately 0.9-msec time delay between the
third turn and the first turn square-wave responses. The
delay corresponds to the travel time that a disturbance

in response magnitude around the characteristic frequency is not matched by the CM. While there is an

must

unmistakable rise in the response in the CM (especially

motion of the stapes generates a square pressure wave

at the oval window which in turn, produces an up and

when measured at low signal levels as we will discuss

later) this rise falls far short of its mechanical counter-

take

to move

between

the two electrode

locations

(about 10 mm). It can be considered that the triangular

down (square) displacement of the cochlear partition.

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601

Dallos,Cheatham,and Ferraro:Cochlearmechanicsand potentials

T2

I T

any given graph, and response functions are obtained for a

range of displacement values. These values are indi-

TI

30

ioooI_40

catednextto the plots.in decibelsrelative to 1 .

40

Not

the entire frequency range is covered for any of the

plots, instead the graphs depict the CM behavior over
the most critical frequency region which is around the
peak of the functions. There are a number of significant

30
20

300 - 20
I

601

observations

" IOO

that

can be made

about

these

families

of

plots, and the observations apply equally to recordings

obtained from any cochlear turn. At the lowest input
levels there is very little change in the shape of the CM
functions with an increase in stimulus strength.
Con-

3o

sequentlyat all frequencies an approximately 10 dB increase in CM magnitudeaccompaniesa 10 dB increase

I0-

O.2 0.

'r

O.5

I0

20

Frequency

FIG.

5.

{ kHz)

CM versus frequency plots from three individual

guinea pigs having electrodes in three different turns, one (T1)

two (T2), and three (T3). Plots are obtained at different, constant, values of stapes displacement.

The latter is indicated as

theparameterin dBre I

This square displacement wave travels along the cochlear partition producing the square-wave-like
CM,

which, as yon B&k&syhas shown, is proportional to the

displacement of the partition.

Lest it is inappropriately generalized, it might be

worth pointing out that the above arguments apply to the

guinea pig and might not be completely transferable to

other species. Thus for example, the CM functions obtained at a constant stapes velocity are not flat in the
cat or in the chinchilla. Instead, these functions decline at a rate of 6 dB/octave as frequency is lowered
below approximately 100-200 Hz. Similarly, when the

stapes of the chinchilla is moved by a triangular displacement, the resulting CM is not a pure square wave
but it possesses pronounced impulse components at the
transitions. We have suggested some years ago that
these discrepancies simply reflect the varied influence

of the helicotremauponcochlear response (Dallos, 1970).

The helicotrema is a high-pass filter as far as basilar
membrane displacement is concerned, and the Cornerfrequency of the filter is species dependent. In animals

with relatively small helicotremas (e.g., guinea pig) the

corner frequency is very low and thus in the usual range
of frequencies the helicotrema exerts no significant effect.

In contrast, in those species where the helico-

in stapes displacement. Stated another way, at low

levels the plots would superimpose if shifted vertically
by appropriate multiples of 10 dB. As intensity increases one notes that the shape of the plots is altered.
The alteration involves the shift of the peak toward the

lower frequencies, the bunching of the graphs immediately above the frequency of the low-level peak, and actual

decreases
in response
withincreasedinput-againjust
above the original peak. The pronounced shape changes
in the plots with intensity indicate that only at the lowest
stimulus levels can one presume that nonlinear effects
negligibly influence the CM response. Some departures

fromlinea.rityoccuraboveapproximately
1 . of stapes
displacement.' This meansthat whentranslatedinto the
more familiar sound-pressure measure, one can not
expect truly linear CM response from the third cochlear
turn above 30 dB SPL, from the second above 55 dB,
and from the first above 75 dB. Early onset of nonlinearity, however, occurs in a rather limited frequency region: just above the best frequency of the electrode location. Far distant from this region the response remains markedly linear up to extremely high driving

levels. Recordingfrom the first cochlearturn (or

from the round window) and using relatively low test
frequencies thus gave rise to the many statements that
can be found in the literature

that indicate

that except

for very high levels the CM is a linear function of sound

intensity. Clearly, when test frequencies most appropriate for a given electrode location are used, that
is frequencies nearest to the peak, and when the low-

pass filtering effect of the middle ear is eliminated,

then it becomes quite evident that the CM is far from

being a linear.response.

To further amplify these con-

tentions in, Fig. 6 the constant stapes displacement CM

plots obtained from the basal turn of one guinea pig are

trema is large (e.g., cat) the corner frequency is well

within the audio range (100-200 Hz) and the filter effect

recast in a normalized fashion. In other words, each

plot is given a vertical translation equivalent to an ex-

is manifested by the decline of the low-frequency response and the departure from the rule that the CM is
proportional to stapes velocity.

pected linear increase commensurate with the increase

in the input. Under such graphing procedures plots that
depict linear changes in CM superimpose, whereas nonlinear changes are signified by the downward shift of
data points. The more pronounced the nonlinear effect,

We have stated previously that the nonlinear nature of

CM-production can influence the various CM versus frequency contours that we have been examining. The best
means of demonstrating such nonlinear effects is to present CMmagnitude functions at several values of the constant input parameter. In Fig. 5 families of CM versus

the further the departures are from superposition. The

plots of Fig. 6 vividly show that at low frequencies the
nonlinearity is negligible since all curves superimpose.
Above the best frequency the nonlinearity is marked
and there are wide departures among the plots.

Above

frequency
plotsare shownfor three electrodelocations.

this region the spread of the curves decreases again

In these plots the stapes displacement is kept constant for

signifying the lesser nonlinear influences.

As a means

J. Acoust.Soc. Am., Vol. 55, No. 3, March 1974

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602

Dallos,Cheatham,
andFerraro:Cochlearmechanics
andpotentials

1.0

602

their primaries then all orders of harmonics and combination tones peak at the same frequency, which depends primarily on the location of the recording elec-

-I0,0
I0

trodes. It is thus sufficient to provide a frequency plot

20

for a single harmonic to i.dicate the general frequency

dependence of any CM distortion component. In Fig. 7
three pairs of plots are given for fundamentals and second harmonics measured at the constant stapes displace-

50

ment of 10 from three electrode locations. The fundamental plots show the now familiar steady growth toward
a peak and the subsequent rapid decline. The animals
were chosen to be representative, thus the differences
in magnitudes from turn-to-turn that are seen here are
a reasonably consistent finding. Accordingly the peak
response tends to be the greatest in the second turn and

0.01

0.1

02 0.

0.5

I0

Frequency

20

(kHz)

FIG. 6. Normalized CM magnitude versus frequency functions

obtained at different stapes displacement values (parameter is

stapesdisplacement
in dBre I ). Plotsarefromoneindividual guinea pig, recording is from the basal turn. In the lower
plot a "degree of nonlinearity" function is presented. This
function is defined by the ratios of the normalized CM mag-

nitudesat I and10 . stapesdisplacements

at differentfrequencies.

smallest

in the first

turn.

The second

harmonic

func-

tions show a very similar ranking in peak magnitude,

and their position along the frequency scale is clearly
determined by the maximum of the fundamental plot. It
is emphasized that the second harmonic functions are

plotted at the frequency of the fundamental, that is, the

magnitude of the second harmonic component (e.g.,

800 Hz) in the CM responseis plottedat the frequency

of the eliciting fundamental (e.g., 400 Hz).

of quantifyingthese contentionswe now introducea "degree of nonlinearity function." This function is obtained
by forming the ratio between the normalized magnitudes
of any two CM plots. For convenience we choose the

ratio betweennormalizedCM at 1 and 10 stapesdisplacements and present the resulting function on the bottom of Fig. 6. A value of one indicates linear response,
and the more nonlinear the CM becomes the larger the
numerical value of the function. It is apparent that we
have a rather sharply peaked plot whose maximum occurs at 14000 Hz, somewhat above the peak of the lowlevel CM .function. Highly similar functions can be obtained

from

the other

cochlear

The fact

that the harmonic and fundamental plots peak at the

same frequency indicates that the distortion components
are not mediated by traveling waves. The distortion
components are always confined to a much narrower

frequency region than the primaries; to state it differently, they show sharper tuning. This suggests that the
distortion component amplitude is not a simple function
of the magnitude of the primary CM, or of the input
stapes displacement.
It is worth reemphasizing that
all orders of distortion

components show identical fre-

quency dependence, that is they are all confined to the

turns.

T$

T2

It is tempting to associate the pronounced frequencydependent nonlinearity of the CM with the somewhat simi-

lar nonlinearity that Rhode (1971) has observed in the

basilar membrane motion. Militating against this temptation are numerous observations supporting the claim that
the dominant CM nonlinearity arises from hair cell pro-

cesses, that is, from distortion tied in with the transducer mechanism as opposed to hydraulic or mechanical

processes occurring prior to transduction (Dallos et al.,

1969; Durrant and Dallos, 1972a, b).
Distortion components measured in the CM are the
primary indicators of the nonlinearity of this electrical
phenomenon. It has been our observation that all CM
distortion components, that is, harmonics and intermodulation components of any order, behave essentially

in the same

manner.

This

behavior

,,

,,
i
i

can be summarized

by noting that these distortion components show growth

patterns as if a simple polynomial nonlinearity would
have generated them, and that irrespective of their order
they are all localized in the same region of the cochlea

(Sweetmanand Dallos, 1969; Dallos and Sweetman,

1969; Worthington and Dallos, 1971; Dallos, 1969a;
Dallos, 1973). Thus if plotted at the frequency of their
eliciting fundamental or at the average frequency of

O.

0.1

I
0.

0.5

,5

Frequency

13

I0

20

(kHz)

FIG. 7. CM magnitudes from three different turns (different

animals)as thefunction
of frequency
at a constant
10 stapes
displacement. Both fundamental (solid symbols) and second
harmonic components (open symbols) are shown. The second
harmonic functions are plotted at the frequency of the fundamental.

J. Acoust. Soc. Am., Vol. 55, No. 3, March 1974.

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603

Dallos,Cheatham,
andFerraro:Cochlear
mechanics
andpotentials
i

3o

AVE(10.)

603

ti0n. Thus while the absolute magnitude of the distortion component is greatest at the frequency where the
fundamental CM is maximum, the relative distortion is
most pronounced where the degree of nonlinearity is the

largest.

As a final comparison, in the right panel the

DIF andAVE SP components

obtainedat 10 . stapes
displacement are also shown. Well defined peaks of
both DIF' and AVE* occur between 3000 and 4000 Hz.
I0

"'

SECOND
TURN
.I

.-.

These peaks are clearly better correlated with the frequency region of greatest nonlinearity than with the
fundamental

CM

maximum.

oJ- I \ !!

%2fo
(10,)-j3o
.

{ ?_fj,.)'
'1I i

The final nonlinear phenomenon in need of a brief discussion is the elusive "interference
effect."
First noted

by Black and Covell (1936) and studied by Wever et al.

(1940), Engebretson and Eldredge (1968), Worthington

(1970) and most recently by Legouix et al. (1973), inter-

i0 .

ference is an effect whereby the CM response to one

(")

3 '

tone

-30

is diminished

when

a second

tone

is introduced.

It

was first suggested by Engebretson and Eldredge (1968)

FIG. 8. left panel: CM magnitude functions at constant i and

that interference is a nonlinear effect that is intimately

tied to combination tone production and summating potential generation. We have extended these ideas and also
demonstrated a pronounced interference effect on the

10 stapesdisplacement
as thefunction
of frequency.Both

summatingpotential itself (Durrant and Dallos, 1974).

0.31
I

, ,, &,,,
2

, I,

, ,,11
5

Frequency (kHz)

-I00
I

2 3

I I

5 7

fundamental(f0) and secondharmonic components(2f0) are

shown. These recordings are obtained from electrodes situated
in the second turn of the cochlea.

The vertical

interrupted

line in all three panels is drawn at the frequency (2500 Hz)

where the low-level fundamental CM plot peaks. middle panel:
Plots of degree of nonlinearity function (DON) obtained as the

ratioof thenormalized
CMmagnitude
at i and10 stapesdisplacements,
andthepercent
second
harmonic
content
at 10
stapes displacement.

right panel: DIF and AVE SP obtained at

constant
10 stapesdisplacement.All measurements
are from
the same

animal.

same narrow frequency band in the proximity of the best

frequency of the recording electrodes.

While the absolute magnitude of the various distortion

components tends to peak at the same frequency where

We would how like to demonstrate

that interference

effects occur in the.same general frequency region

where all other nonlinear phenomena are seen to be
profninent, namely at and above the frequency of the
maximum of the CM function for any given electrode
location. Our contention is that the CM of any stimulus
frequency that is transduced by a given cochlear region
can be interfered with, but that all the effective interfering frequencies are at or above the best frequency
of that region. These statements can best be explained
with the aid of Fig. 9. In the left panel of the figure a
sample interference plot is shown to demonstrate the
effect. Here the probe tone (the tone whose CM is subject to interference) is 7000 Hz (arrow) presented at a

stapesdisplacement
of 1 .

The interferingtone'sfre-

quency is varied while its level is maintained at a con-

the fundamentalis maximum, adifferentpictureemerges

stantstapesdisplacement
of 10 ,. The ordinateshows

when the percent distortion is plotted as a fun(tion of

the level of the 7000 Hz CM component as the function

of the frequency of the interfering tone. It is evident
that interference takes place within a relatively narrow
frequency band only, that the frequency dependence is
quite sharp, and that a very significant decrease in the
measured CM can be induced by relatively moderate
intensity interfering tones. An interesting and rather
unexpected finding is that the frequency of maximal

fundamentalfrequency. To aid in demonstratingthe difference and [o provide a summary of much of our previous discussion Fig. 8 is presented. In this figure various plots, all obtained from one animal, are given. In
the left panel, fundamental and second harmonic magni-

tudefunctionsare shownfor both I and 10 . stapesdisplacements.

These plots demonstrate already familiar

features. The I . fundamental

functionpeaksat 2500

interference (dip-frequency) is a function of not only the

Hz (second turn electrodes) and this is the frequency of

the peaks of both second harmonic functions as well. The

electrode location but also of the probe frequency.

In
the right panel of Fig. 9 data are combined from three
animals, all having electrodes in the,first turn of their
cochleas, to show the relationship between dip and
probe frequencies.
A systematic functional relationship is strongly suggested by the data. It seems that
no matter what the probe frequency is, strong interference does not occur at frequencies that are significantly

10 . fundamental
CM graphshowsthe signsof marked
nonlinear influences. The peak shifts down to 1250 Hz,
and a dip develops at 3500 Hz. In the center panel the
degree of nonlinearity function clearly indicates that the
most nonlinear frequency region is between 3000 and
3500 Hz. This region is above the low-intensity fundamental peak of 2500 Hz. Also included in the center
panel is a plot showing the percent second harmonic dis-

tortionat 10 . stapesdisplacement. This plot hasvirtually the same shape as the degree of nonlinearity func-

below the best (peak) frequency of the electrode location.

In this case, the lowest peak frequency was at 9000 Hz.
At higher probe frequencies, however, the dip frequency
is systematically increased according to an approximate-

J. Acoust. Soc. Am., Vol. 55, No. 3, March 1974

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604

Dallos,Cheatham,
and Ferraro:Cochlearmechanics
andpotentials
25

occurs somewhat above the best frequency, when the

latter is defined as the frequency of the peak in the CM
versus frequency plots when obtained at very small
stapes displacement.
It is shown that the relative
amount of harmonic distortion present in the CM is
well correlated with the region of most pronounced non-

20
'E

0.3

604

linearity, and the DIF' and AVE + summating potential

._

0.03

I0

20

left panel:

I0

15

Probe tone frequency

Interference tone frequency

FIG. 9.

20

(kHz)

Relative magnitude of the CM in response

to a 7000-Hz(arrow)tonepresented
at I stapesdisplacement
level as the functionof thdfrequencyof an interferingtonewhich

is presented
at a constant
stapesdisplacement
of 10. Recording is from the first turn; right panel: Combined data
from three animals showing the relation between the frequency

of the most pronouncedinterference (dip frequency) and the

frequency of the tone that is interfered with (probe frequency).
All data are based on first

turn recordings with probe fre-

components peak in this very region as well. Finally,

it is demonstrated that irrespective of the frequency

of a tone, maximaltonalinterferencewith its CM occurs above the best frequency associated with the location of the recording electrode, in other words in the
aforementioned maximally nonlinear frequency band.
ACKNOWLEDGMENT

This work is supported by several grants from the

National Institute of Neurological Diseases and Stroke,
NIH.

quencies
presented
at constant
I , andinterfering
frequencies
at constant
10 stapesdisplacement..
*It is likely that above approximately 20 kHz the cutoff rate
becomes considerably greater.

ly linear rule. The mechanism underlying this relationship is not at all evident, it is, however, quite clear
that effective interference

occurs when the interfering

tone is within a region where our "degree of nonlinearity" function is large. It is interesting to note that we
never see significant interference below the best frequency, thus we can not confirm the existence of the
double-lobed

interference

functions

that have been re-

cently reported by Legouix et al. (1973) which they

have likened to the frequency behavior of the two-tone
suppression in single unit responses. R is not apparent
why our results are in conflict.

The primary concentration of all nonlinear effects

that are measurable in cochlear potentials to the frequency region at and above the best frequency of a given
electrode

III.

location

is thus a well

demonstrated

fact.

SUMMARY

In this communication we are primarily concerned

with considering how nonlinear effects influence the
properties of CM tuning curves. It is pointed out that
the CM recorded

from

normal

cochleas

is overwhelm-

ion the basis of a sizable number of animals from which we

obtained both electrophysiological and histological data, it is
estimated that the sensitivity difference between outer and
inner hair cells ranges between 30 and 40 dB.

2Aquite consistentobservationis that the earliest onsetof

nonlinearity occurs in the second turn followed by the third
turn, while the first turn response maintains its linearity
up to higher driving levels. The examples of Fig. 5 clearly
demonstrate this progression.

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