The
Fetus
& & & & & & & & & &
The Acoustic Environment and Physiological Responses of the
Fetus
Robert M. Abrams, PhD
Kenneth J. Gerhardt, PhD
The acoustic environment of the fetus is composed of continuous
cardiovascular, respiratory, and intestinal sounds that are punctuated by
isolated, shorter bursts during maternal body movements and vocalizations.
The distribution of sounds is confined to frequencies below 300 Hz.
Additionally, vibrations on the external surface of the maternal abdomen
can induce sounds inside the uterus. The half - round sound pressure
contours in the abdomen during vibroacoustic stimulation differ from the
circular distribution of contours resulting from airborne sound pressure
exposure. The static and dynamic forces of the vibrator and the vibrator
distance from the target are also factors in sound transmission. Responses
to sound are best described in animals and include changes in behavioral
state, brain bloodflow, auditory brainstem response, and local cerebral
glucose utilization along the central auditory pathway.
Journal of Perinatology 2000; 20:S30 ± S35.
INTRODUCTION
In a 1985 inventory of progress of research on energy metabolism
during prenatal development,1 we drew attention to some recent
studies in pregnant sheep that had modified our understanding of
the circulatory and metabolic requirements for maturation and
growth of the fetal brain. Among the most significant developments
reviewed at that time was the finding of very high rates of glucose
utilization all along the fetal central auditory pathway under normal
ambient sound conditions.2 Consequently, even higher rates of
energy metabolism were noted during external noise stimulation.3
These findings paralleled in time the development by obstetricians
of a test for assessing fetal health that took advantage of fetal audition
during prepartum and intrapartum examinations.4 Pregnant women
have been quite aware that their fetuses moved in response to loud
noises, but these anecdotal observations generated little more than
passing comment in the published literature prior to the decade of the
1980s. However, with the introduction of real-time ultrasonography,
Department of Obstetrics and Gynecology (R.M.A., K.J.G.), University of Florida, Gainesville, FL;
Department of Pediatrics (R.M.A.), University of Florida, Gainesville, FL; Department of
Communication Sciences and Disorders (K.J.G.), University of Florida, Gainesville, FL.
Address correspondence and reprint requests to Kenneth J. Gerhardt, University of Florida, 338
Dauer Hall, Box 117420, Gainesville, FL 32611.
S30
& & & &
the non-invasive examination of fetal physiologic responses to
sounds became possible. The fetal vibroacoustic stimulation (VAS)
test quickly became a popular adjunct to the traditional fetal non-
stress test.5,6 The objective of the test is to note a stimulus-linked
increase in fetal activity, as judged by cardioacceleration.
During subsequent years, a third area of interest developed
among psychobiologists. As a result of their research, the rich and
varied sound environment within the uterus is now believed to
contribute to fetal learning.7,8
Finally, the possibility that overexposure to noise, primarily in the
workplace, may place the fetus at risk for hearing loss has become a
focus of the research community.9 This latter issue has received scant
attention in spite of the fact that the number and the proportion of
women in the reproductive age group in the labor force have
increased markedly in the last several decades.10 In 1994,
approximately 75% of women in the prime child-bearing years
(aged between 24 and 35 years) was in the labor force.
Occupational Safety and Health Administration regulations do
not address fetal exposure limits, nor are there guidelines regulating
the noises present when fetuses are born prematurely and must live,
often for extended periods of time, in intensive care nurseries and in
conditions of altered acoustic stimulation. Existing recommenda-
tions by other groups for nursery noise levels are reviewed later in
this issue.
During the 1960s, a few researchers began to study the
transmission of sounds from the mother's environment into the
uterus. Their interest was in describing the extent to which the
fetus was able to react to the exogenous sound environment.
Bench,11 using a microphone covered with a rubber sleeve,
measured the attenuation of sounds across the maternal
abdomen. Sound pressures were significantly attenuated across
the audible frequency range, with the greatest loss in energy in
the higher frequencies. The author concluded that human
fetuses develop in an environment devoid of sounds. This notion
has become part of the general knowledge base, and
consequently, little research was conducted in this area in the
decade of the 1970s following Bench's publication. In
subsequent studies,12 it was pointed out that instrumentation
constraints probably distorted the data cited above, and studies
were repeated with a more appropriate transducer intended for
underwater sound measurements Ð the hydrophone.
A number of conditions must be met in order for the fetus
to detect an acoustic stimulus from outside its mother. The
Journal of Perinatology 2000; 20:S30 ± S35
# 2000 Nature America Inc. All rights reserved. 0743-8346/00 $15
www.nature.com/jp
Acoustic Environment and Physiological Responses Abrams and Gerhardt

Obstetricians often use an EAL as a sound source to elicit a

response from the fetus as part of a procedure to assess fetal health.
The EAL is a small, handheld device that was originally designed for
use by alaryngeal talkers. The physician places the EAL diaphragm
on the abdomen of the pregnant woman. When activated, it produces
an acoustic signal in the uterus that has peak energy from 0.5 to 1.0
kHz and may reach over 129 dB SPL at the fetal head.15 In sheep, the
level of the EAL recorded directly over the fetal head has been
recorded as high as 135 dB.12 As seen in Figure 2, specification of the
SPL in air Ð a common practice in clinical studies in obstetrics16
Ð is not helpful in inferring the true stimulus present at the fetal
head in utero. The EAL produces excitation by a short-duration
impact with a fundamental frequency of less that 100 Hz and
multiple overtones of significant amplitude.17 The use of calibratable
hydrophones is essential for quantitation of SPL in tissues; use of
condenser, air-filled microphones is not advised.18
Figure 1. Average intrauterine sound pressure level before ( open bars )
Experiments with sheep19 have documented the importance of
and after (solid bars ) death of ewe and fetus.
specifying the dynamic and static forces of the vibrator, as well as the
distance to the target, in this case the fetus. Distance to the fetal head
may not be as great a factor in the human15 because of the relatively
cochlea and neural pathways must be functional. This occurs in
larger size of the head compared to the abdominal segment.
the human fetus during the beginning of the third trimester.
It is the frequency of sound input, however, that mostly
The stimulus must have energy in frequency bands that exceed
determines the SPL in the uterus.19 ± 21 During VAS at 10 and 100
the background noise floor in that same frequency band. The
Hz applied with a mechanical shaker, the intra-abdominal
intensity of the exogenous stimulus must generate a sufficient
isosound pressures (lines of equal SPL) were fairly flat in all
sound pressure to penetrate the uterus. The energy at the fetal
directions, whereas the contours produced by 2000 Hz were
head needs to produce mechanical displacements of the basilar
decidedly curved19 (Figure 3). The overall shapes of these
membrane of the organ of Corti in order for hair cells and
pressure contours revealed important differences in the manner
associated afferent neurons to be triggered. Finally, the response
in which acoustic signals pass through the abdomen. These
of the fetus to acoustic stimulation must be sampled in order
hemicentric sound pressure contours introduced by VAS were very
to quantify the nature of the stimulus that reaches the hearing
different, with respect to absolute levels and overall attenuation,
mechanism. These responses take different forms and will be
described more thoroughly later in this chapter. The reader is
directed to the paper by Gerhardt and Abrams in this volume
for related data on fetal exposure to sound stimulation and
VAS.
It is by no means quiet in the uterus. Internal sounds result
mainly from maternal cardiovascular, respiratory, and intestinal
sources. These more or less continuous sounds are punctuated by
isolated, short bursts during maternal body movements and
vocalizations.13 As seen in Figure 1, much of the differences
between the sound pressure level (SPL) in the uterus of a living
ewe and a euthanized ewe is confined to 1/3 octave bands below
300 Hz.

CLASSES OF FETAL STIMULATION

VAS
Acoustic stimulation occurs either as vibroacoustic, i.e., through
vibrating instruments or machines placed in contact with the
external surfaces of the body, or through airborne means. Figure 2. One - twelfth octave band spectra of an EAL. Open bars: SPL
Vibroacoustic stimulators, such as an electronic artificial larynx recorded with an intra -abdominal hydrophone. Solid bars: SPL recorded in
(EAL), produce high levels of sound (SPLs in decibels).14 air, not in contact with skin. All SPL values refer to 20 Pa.

Journal of Perinatology 2000; 20:S30 ± S35 S31

 Abrams and Gerhardt
Figure 3. Isosound pressure contours ( lines of equal SPL ) for four
different frequencies; A ±D, cross - sectional plane through the abdomen of
a standing nonpregnant sheep just below the umbilicus. The point of
midline VAS is designated by the reference point, 0. Reprinted with
permission.19
from the circular distribution of contours resulting from airborne
sound exposure.22
The effect of distance to target is illustrated also in experiments in
which hydrophones were placed at 45 intra-abdominal locations in
Figure 4. One - twelfth octave band spectra in response to bowing an open
G-string of a double bass held against the flank of a standing ewe. A.
Spectrum recorded in air 0.5 m from the bridge of the instrument. B.
Spectrum recorded in utero with a miniature hydrophone attached to the
head of the fetus. Reprinted with permission.23
S32
Acoustic Environment and Physiological Responses
sheep.19 While sine wave vibrations were used in the experiments
mentioned above, the effect of vibration frequency is easily
demonstrated with complex vibratory-induced sounds, such as
might be experienced while in physical contact with a double bass23
(Figure 4). Note the reduction in level of higher-frequency partials
in the spectrum recorded from the uterus compared to the spectrum
recorded in air.
Other examples of non±air-induced acoustic stimuli in the
uterus are mother's voice Ð the most significant and common
mode of potential auditory stimulation Ð and also contact with
vibrating objects at work or play.
Airborne Stimulation
Note that many years ago, the dominant opinion of society was that
the fetus lived isolated from the noise of the world.24 The pioneering
work of Querleu et al.,25 summarized in a review in Seminars in
Perinatology, provided the first detailed description of the
characteristics of the acoustic environment of the human fetus. These
investigators found that human voices emerge above the basal noise,
and that the male voice is better transmitted and only slightly
attenuated due to its lower pitch. A perceptual analysis of isolated
word segments was made using the usual criteria of speech
audiometry. Listeners could recognize 30% of over 3000 French
phonemes. Listeners also determined that the voiced features of a
French lullaby Ð a tune chosen for its simplicity of form and
Figure 5. Cross section isoattenuation contours within the sheep
abdomen. Airborne broadband noise was delivered to the left flank and
recorded intra - abdominally. Attenuation contours of four selected
frequencies are displayed. Reprinted with permission.22
Journal of Perinatology 2000; 20:S30 ± S35
Acoustic Environment and Physiological Responses
content Ð proved the exact reproduction of the intonation in the
ex utero recorded segments.
Griffiths et al.26 carefully examined the intelligibility of
phonemes recorded in air versus those recorded in utero in the
pregnant sheep. There are three important features that contribute
to the understandability of speech. ``Voicing'' features refer to the
presence or absence of vocal fold vibrations (e.g., p versus b);
``place'' of articulation refers to the location of major constriction
in the airflow (e.g., bilabial versus glottal); and ``manner'' of
articulation refers to the method of production (e.g., plosive
versus fricative). An analysis of the feature information
transmitted into the uterus from recordings of speech revealed that
voicing information is better transmitted than the features of place
and manner. Poorer in utero reception of information about the
place and manner of articulation as compared with voicing
features is associated with losses of higher-frequency sound
pressures.27 This is consistent with the prediction that transmission
into the uterus can be modeled as a low-pass filter, i.e., high-
frequency energy is reduced in amplitude.18
Experiments with sheep Ð a good animal model for human
studies because of similarities in the physics of transmission and
the early development of inner ear function prenatally Ð showed
that the attenuation of airborne sounds are highly frequency-
dependent,22 resulting in isosound pressure profiles similar to those
seen in Figure 5.
FETAL PHYSIOLOGICAL RESPONSES TO SOUNDS
Studies in Humans
Fetal breathing and body movements. A variety of stimulators
has been used to evoke fetal movements, but the most popular has
been the EAL, which is held against the abdominal wall for a few
seconds. Gagnon 4 noted that in fetuses aged between 33 and 40
weeks, there was an increase in gross fetal movements which began
10 minutes after a 5-second stimulation with a vibroacoustic
stimulator and persisted up to 1 hour. However, in fetuses between 26
and 32 weeks of gestation, gross fetal movements were not altered by
the stimulus.
Fetal breathing activity was altered only in fetuses aged between
36 and 40 weeks. Following stimulation with an artificial larynx, the
incidence of fetal breathing movements immediately decreased and
breathing activity became more irregular for a period of up to 1
hour.
Fetal heart rate responses. Following a 5-second vibroacoustic
stimulus to the abdominal surface of selected women volunteers
between 33 and 40 weeks of gestation, there was a report of fetal
tachycardia that persisted up to 1 hour.4 Often, the onset of the
response was delayed between 10 and 20 minutes.
Behavioral states. Heart rate and heart rate variability, eye
movements, breathing movements, mouthing, sucking, micturition,
Journal of Perinatology 2000; 20:S30 ± S35
Abrams and Gerhardt
and hiccups are variables that are easily recognizable and have a
well-defined association with one another during the third trimester
of pregnancy. Fetal behavior at this time is very similar to neonatal
behavior, and a classification of four cyclic ``states'' has been
developed to aid those interested in evaluation of fetal health.28 The
issues of the dramatic state changes that occur during VAS are
discussed by Visser and Mulder29 and Zimmer and Divon.30
The human fetal response to vibroacoustic stimulation has been
studied extensively by obstetricians interested in increasing fetal
heart rate reactivity, which is one marker of fetal health.4 Heart rate
variability has been used successfully by developmental psycho-
biologists to study some aspects of fetal learning, including
habituation.31
Hearing. Not only are there physical differences between acoustic
stimulation and VAS, but the responses of the fetus are also different.
Greater heart rate acceleration and more vigorous changes in fetal
movements are obtained with VAS.32 These differences may be
accounted for because the stimulus levels delivered to the fetal head
are so much greater during VAS than during acoustic stimulation.
Because the stimulus levels of the VAS are so high, a number
of investigators have studied the hearing of children whose
mothers had undergone VAS testing while pregnant with them.33 ± 35
Hearing was assessed using click-evoked auditory brainstem
responses (ABRs). No differences were found between these
children and age-matched controls that did not receive VAS
during fetal life. Although permanent hearing impairment, as
measured with click-evoked ABR, does not appear to be a risk
factor associated with VAS testing, Visser and Mulder29 offered a
cautionary note when they described the effect of the EAL on fetal
behavioral state organization. It was concluded that stimulation
induced excessive fetal movements, prolonged tachycardia, non-
physiological state changes, and disorganization and change in
the distribution of fetal behavioral states. The authors warned
against routine testing using the EAL because of these unusually
dramatic state changes in the fetus.
Studies in Animals
Most animal studies of fetal response to sounds have involved
preterm pregnant sheep. Indices of response include the following.
ABRs. Griffiths et al.36 described the technique which showed that
sounds can penetrate the uterus and result in alterations of the fetal
ABR. In this study, the ABR was used as an index of noise-induced
hearing loss.
Local cerebral glucose utilization. High-intensity sound
stimulation resulted in significant increases in glucose utilization in
the central auditory pathway structures in sheep fetuses.37
Fetal behavioral state. Measurement of fetal cortical activity and
orbital and neck muscle potentials during VAS of the abdomen of
S33
 Abrams and Gerhardt
a pregnant ewe clearly showed a disruption of fetal behavior
state.37,38 In other studies,39 it was found that local cerebral
bloodflow changed markedly during natural alterations in fetal
behavioral state.
CONCLUSIONS
The acoustic environment of the human fetus is rich and varied.
Limitations on the spectral experiences are afforded by the air±tissue
interface and by the transmission of sounds favoring those in
frequency bands below 200 to 300 Hz. In many cases, fetuses respond
to environmental sounds as evidenced by changes in variables
associated with behavioral state, such as heart rate variability and eye
and breathing movements. Animal experiments have been useful in
defining transmission characteristics and physiologic responses.
Subtle influences of acoustic stimulation in human fetuses suggest a
prenatal development of human behavior. How behavioral
development is modified when infants are prematurely delivered and
are placed in an environment outside the uterus is a question
requiring more research and discussion.
References
1. Abrams RM, Hutchison AA. Energy metabolism of the developing brain. J
Reprod Med 1985;30:318 ± 323.
2. Abrams RM, Ito M, Frisinger JE, Patlak CS, Pettigrew KD, Kennedy C. Local
cerebral glucose utilization in fetal and neonatal sheep. Am J Physiol
1984;246:608 ± 618.
3. Abrams RM, Hutchison, AA, Gerhardt KJ. Effect of high - intensity sound on
local cerebral glucose utilization. Dev Brain Res 1989;48:1 ± 10.
4. Gagnon R. Stimulation of human fetuses with sound and vibration. Semin
Perinatol 1989;13:393 ± 402.
5. Serafini P, Lindsay MBJ, Nagey DA, Pupkin MJ, Tseng P, Crenshaw C.
Antepartum fetal heart rate response to sound stimulation: the acoustic
stimulation test. Am J Obstet Gynecol 1984;148:41 ± 45.
6. Smith CV, Phelan JP, Paul RH, Broussard P. Fetal acoustic stimulation
testing: a retrospective experience with the fetal acoustic stimulation test. Am
J Obstet Gynecol 1985;153:567 ± 568.
7. Fifer WP, Moon CM. The effects of fetal experience with sound. In: Lecanuet
J - P, Fifer WP, Krasnegor NA, Smotherman WP, editors. Fetal Development: A
Psychobiological Perspective. Hillsdale, NJ: Lawrence Erlbaum Associates
Publishers; 1995. pp. 351 ± 366.
8. Lecanuet J - P, Gautheron B, Locatelli A, Schaal B, Jacquet AY, Busnel MC.
What sounds reach fetuses: biological and non - biological modeling of the
transmission of pure tones. Dev Psychobiol 1998;33:203 ± 219.
9. Gerhardt KJ, Pierson LL, Huang X, Abrams RM, Rarey KE. Effects of noise
exposure on fetal sheep auditory brainstem response and inner ear histology.
Ear Hear 1999;20:21 ± 32.
10. Shehan CL. Sociodemographic perspectives on pregnant women at work.
Semin Perinatol 1996;20:2 ± 10.
11. Bench RJ. Sound transmission to the human foetus through the abdominal
wall. J Gen Psychol 1968;113:85 ± 87.
12. Gerhardt KJ, Abrams RM, Kovaz BM, Gomez KJ, Conlon M. Intrauterine noise
levels produced in pregnant ewes by sound applied to the abdomen. Am J
Obstet Gynecol 1988;59:228 ± 232.
S34
Acoustic Environment and Physiological Responses
13. Abrams RM, Gerhardt KJ, Griffiths SK, Huang X, Antonelli PJ. Intrauterine
sound in sheep. J Sound Vib 1998;216:539 ± 542.
14. Abrams RM, Schwab M, Gerhardt KJ, Bauer R, Peters AJM. Vibroacoustic
stimulation with a complex signal: effect on behavioral state in fetal sheep.
Biol Neonate 1996;70:155 ± 164.
15. Nyman M, Arulkumaran S, Hsu TS, Ratnam SS, Till O, Westgren M.
Vibroacoustic stimulation and intrauterine sound pressure levels. Obstet
Gynecol 1991;78:803 ± 806.
16. Abrams RM, Gerhardt KJ, Richards DS, Peters AJM. Fetal vibroacoustic
stimulation test: features of the stimulus. Fetal Matern Med Rev 1995;7:87 ±
97.
17. Oliver CC. Sound and vibration transmission in tissues. Semin Perinatol
1989;13:354 ± 361.
18. Gerhardt KJ, Abrams RM, Oliver CC. Sound environment of the fetal sheep.
Am J Obstet Gynecol 1990;162:282 ± 287.
19. Peters AJM, Abrams RM, Gerhardt KJ, Burchfield DJ. Vibration of the
abdomen in non - pregnant sheep: effect of dynamic force and surface area of
vibrator. J Low Freq Noise Vib 1991;10:92 ± 99.
20. Graham EM, Peters AJM, Abrams RM, Gerhardt KJ, Burchfield DJ. Intra -
abdominal sound levels during vibroacoustic stimulation. Am J Obstet
Gynecol 1991;164:1140 ± 1144.
21. Richards DS, Abrams RM, Gerhardt KJ, McCann ME. Effects of vibration
frequency and tissue thickness on intrauterine sound levels in sheep. Am J
Obstet Gynecol 1991;165:438 ± 442.
22. Peters AJM, Gerhardt KJ, Abrams RM, Longmate JA. Three - dimensional
intra - abdominal sound pressures in sheep produced by airborne stimuli. Am
J Obstet Gynecol 1993;169:1304 ± 1305.
23. Abrams RM, Gerhardt KJ. Some aspects of the foetal sound environment. In:
Deliege I, Sloboda J, editors. Perception and Cognition of Music. East Sussex,
UK: Psychology Press; 1997. pp. 83 ± 101.
24. Lecanuet J - P, Schaal B. Fetal sensory competencies. Eur J Obstet Gynecol
Reprod Biol 1996; 68: 1 ± 23.
25. Querleu D, Renard X, Boutteville C, Crepin G. Hearing by the human fetus?
Semin Perinatol 1989;13:409 ± 420.
26. Griffiths SK, Brown WS, Gerhardt KJ, Abrams RM, Morris RJ. The perception
of speech sounds recorded within the uterus of a pregnant sheep. J Acoust Soc
1994;96:2055 ± 2063.
27. Miller GA, Nicely RE. An analysis of perceptual confusions among some
English consonants. J Acoust Soc Am 1955;27:338 ± 352.
28. Nijhuis JG, editor. Fetal Behavior: Developmental and Perinatal Aspects. New
York: Oxford University Press; 1992. pp. 216 ± 224.
29. Visser GH, Mulder EJ. The effect of vibroacoustic stimulation on fetal
behavioral state organization. Am J Ind Med 1993;23:531 ± 539.
30. Zimmer EZ, Divon MY. Fetal vibroacoustic stimulation. Obstet Gynecol
1993;81: 451 ± 457.
31. Lecanuet J - P, Granier - Deferre C, Jacquet AY. Decelerative cardiac responses
to acoustical stimulation in the near term fetus. Q J Exp Psychol
1992;44B:279 ± 303.
32. Hepper PG, Shahidullah SB. The development of fetal hearing. Fetal Matern
Med Rev 1994;6:167 ± 179.
33. Arulkumaran S, Skurr B, Tong H, Kek LP, Yeoh KH, Ratnam SS. No evidence
of hearing loss due to fetal acoustic stimulation test. Obstet Gynecol
1991;78:283 ± 285.
34. Ohel G, Horowitz E, Linder N, Sohmer H. Neonatal auditory acuity
following in utero vibroacoustic stimulation. Am J Obstet Gynecol
1987;157:440 ± 441.
Journal of Perinatology 2000; 20:S30 ± S35
Acoustic Environment and Physiological Responses
35. Nyman M, Barr M, Westgren M. A four - year follow - up of hearing and
development in children exposed in utero to vibroacoustic stimulation. Br J
Obstet Gynecol 1992;99:685 ± 688.
36. Griffiths SK, Pierson LL, Gerhardt KJ, Abrams RM, Peters AJM. Noise - induced
hearing loss in fetal sheep. Hear Res 1994;74:221 ± 230.
37. Abrams RM, Peters AJM, Gerhardt KJ, Burchfield, DJ. Vibroacoustic
stimulation in fetal sheep: effect on cerebral glucose utilization and
behavioral state. J Dev Physiol 1993;19:171 ± 177.
Journal of Perinatology 2000; 20:S30 ± S35
Abrams and Gerhardt
38. Peters AJM, Abrams RM, Gerhardt KJ. Abdominal vibration alters sleep state
in fetal sheep. J Dev Physiol 1993;19:227 ± 234.
39. Abrams RM, Post JC, Burchfield DJ, Gomez KJ, Hutchison AA, Conlon M.
Local cerebral bloodflow increased in rapid eye movement sleep in fetal
sheep. Am J Obstet Gynecol 1990;162:278 ± 281.
S35