European Journal of Obstetrics & Gynecology GYliE

ELSEVIER and Reproductive Biology 68 (1996) 1-23

Review paper

Fetal sensory competencies

J e a n - P i e r r e L e c a n u e t *a, Benoist Schaal b

aLaboratoire Cognition et D~veloppement, Universit~ Paris V-CNRS ( URA 2143), 28, rue Serpente, 75006, Paris, France
bLaboratoire de Comportement Animal, Station de Physiologie de la Reproduction, INRA-CNRS ( URA 1291), 37380, Nouzilly, France

Received 14 February 1996; accepted 7 June 1996

Al~tract

A growing body of evidence is available about the functioning of fetal sensory systems during gestation. This article aims at
reviewing data concerning (i) the presence of potential sensory stimulation in the fetal milieu, (ii) the sequential functional develop-
ment of the sensory systemsand (iii) physiological and behavioral responses of fetuses to various types of stimulation. Human data
are compared with data collected in other mammalian species. Most studies have investigated auditory and chemosensory(olfactory
and gustatory) responsivenessof the fetus in the second half of gestation. They demonstrate that (i) motor and heart rate responsive-
ness depends on gestational age and characteristics of stimulation; (ii) fetal sensory experience has short- and long-term effects at
morphological, functional and behavioral levels (for example transnatal learning). The clinical consequences of the fetal sensory
functioning are developed.

Keywords: Fetus; Sensory functioning; Vestibular system; Somesthetic system;Olfaction; Gustation; Audition; Vision; Fetal learn-
ing; Behavioral states

1. Introduction developmental psychologists demonstrated that the sen-

Research on fetal sensory development can be seen
from a medical point of view as the result of a scientific
intrusion performed by experimental zoologists and
psychologists into the domain of obstetricians. Indeed,
the first systematic attempts at analyzing fetal responses
to direct sensory stimulation have been conducted in the
auditory domain by obstetricians, long before
psychologists became interested in this question (see
below). These obstetricians had a pioneering attitude at
a time where the dominant opinion was that the fetus
lived isolated from the agitation of the world. But, these
obstetricians were 'supported' by the vast cohort of
pregnant women who had for a long time performed
their own observations. They had noticed that, since
mid-gestation, they could feel the baby they carried jerk
in the womb when a loud noise occurred in their
vicinity.
During the first half of the XXth century,
sory systems of the newborn function at a quite good
level of performance. Since it does not seem plausible
that this sensory functioning has a sudden inception at
birth, this observation raised the question concerning
prenatal development and functioning of the sensory
systems.
The development of ultrasound techniques in the
seventies (cardiotocography, real-time ultrasonography)
allowing the observation of fetal behavior, made possi-
ble investigations of fetal responsiveness to sensory
stimulation. Today obstetricians and developmental
psychologists, although inspired by different motives
(development of diagnostic tools for the former, exten-
sion of knowledge about psychobiological development
for the latter) often work in collaborative programs to
better describe the ontogeny of fetal sensations and
perceptions.
This in utero fetal functioning requires that: (i) there
are potential sources of stimulation in the fetal milieu,

* Corresponding author.

0301-2115/96/$15.00 © 1996 Elsevier Science Ireland Ltd. All rights reserved

PII S030 !-2115(96)02509-2
2 J.-P. Lecanuet, B. Schaal/European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
and (ii) the sensory systems are functional, thus mature
enough, at both peripheral and central levels. Thus, in
the first section of this paper, the fulfilment of these re-
quirements plus the presentation of evidence of fetal
functioning are presented for each sensory system. In
the review of available data we will follow - - except for
the vestibular system which will be included among the
proprioceptive-somesthetic sensitivities - - the develop-
mental sequence demonstrated in comparative anatomi-
cal studies performed in the human species and other
vertebrates. These studies showed that sensory systems
do initiate their maturation according to the following
sequence: somesthetic system, chemosensory systems
(olfaction and gnstation), vestibular system, auditory
system and visual system. In the last section, the conse-
quences (i) for the fetus and (ii) for the newborn of fetal
sensory experiences are considered in the chemosensory
and auditory modalities.
2. Fetal sensory functioning
2.1. Somesthetic and proprioceptive systems
2.1.1. Potential sources of stimulation
Somesthetic and vestibular systems are stimulated in-
separably in most occurrences of fetal life, especially by
fetal and maternal movements. It is quite impossible to
determine to what extent each system contributes to an
observed response. While the amniotic fluid should
cushion the impact of fast maternal motions, the fetus is
exposed to an increasing number of contacts and
displacements as gestation proceeds. There are contacts
with the uterine wall, contacts between hands and body,
hands and face hands and mouth [1]. This last type of
contact may induce sucking behavior as it can be fre-
quently seen by ultrasonographists.
2.1.2. Structural development of sensory transducers
Somesthetic system. The somesthetic system develops
according to a cephalo-caudal pattern. Neuronal free
ending receptors can be found in the mouth and in the
peri-buccal zone as soon as 8-9 weeks GA (gestational
age). Meissner and Pacini corpuscles develop soon after.
Tactile receptors are to be found on the face, the palm
of the hands and the sole of the feet by 11 weeks. By the
15th week they are found on the trunk and proximal
zones of arms and legs and on the whole skin by the 2nd
week [2]. Their density, especially for the free-ending
nerves is greater than in the adult.
Vestibular system. By the 5th week, the otic vesicle
divides in two parts that will become the saccula and the
utricula. The semi-circular canals stem out of the
utricula by the 6th week. On purely morphological cri-
teria the vestibular apparatus is mature by 14 weeks. Af-
ferent connections from the vestibular nerve, starting
well before neuroepithelium differentiation is ended,
stimulate its development.
2.1.3. Evidence of fetal sensory functioning
Somesthetic system. Several clinical interventions in-
cluding a tactile component, and performed during
labor, evoke a significant heart rate acceleration in most
end of gestation fetuses. This has been found during:
fetal scalp blood sampling [31, a 15-s manual pressure on
the scalp [4] and intra-amniotic injection of fluid
through a pressure measurement tube [5]. The only
other source of data is the observations performed by
Hooker [6] and Humphrey [7,8] on non-viable aborted
fetuses during their short extra uterine life in a hot saline
solution. These perinates respond through a movement
to a calibrated light touch to the upper lip as soon as the
end of the 7th week, when nerve endings have not yet
reached the dermis thus suggesting that the neural
plexus function like specific receptors. The whole body
surface - - except for the back of the trunk and the top
of the head, is responsive to touch stimuli by the
13-14th week. Deep pressures manually exerted on the
fetal body through maternal abdominal tissues or vigor-
ous shaking of the uterus evoke large heart rate accelera-
tions that can be accompanied with motor responses
[9,10]. Pressure at fetal head level may evoke accelera-
tions [11] as well as decelerations [12]. A flush of cold
water (4°C) on the fetal face during labor induces a
motor response and a HR (heart rate) increase even
when given during a quiet sleep episode (a poorly re-
sponsive state) [131.
Nociceptive stimulation. Apart from the HR changes
induced by scalp blood sampling, and the startles evok-
ed by contacts with the needle during amniotic fluid
sampling, very little is known about fetal responses to
nociceptive stimulation. It has been shown that endo-
genous opiates B-endorphin and/3-1ipotropin blood con-
centrations are higher after a breech delivery or a
vacuum delivery than after an eutocic and thus sup-
posedly less stressful delivery [14].
Vestibular system. Premature babies start showing
Moro-like responses by the 25th week, a response that
has been described earlier by Hooker [6]. Elliot and
Elliot [151 suggested that during the 5th month, the fetus
starts to orient itself in utero with a kicking-like behav-
ior. Fetus self-orientation has been discussed in relation
to the birth position [16]. A concurrent hypothesis, sug-
gesting the functioning of a central mechanism suppress-
ing vestibular responsiveness, has been raised [17]. This
mechanism would prevent the fetus from responding to
every maternal motion. Recent data from our group
demonstrate that, by the end of gestation, fetuses
display HR changes in response to maternal passive
rocking and swaying, the nature and the amplitude of
the change depending on the duration of the motion
[181.
 J.-P. Lecanuet. B. Schaal/ European Journal of Obstetrics& Gynecologyand ReproductiveBiology68 (1996) 1-23
2.2. Chemosensory systems ( olfaction and gustation)
2.2.1. Potential sources of stimulation
The amniotic fluid is the most obvious mediation of
potential chemical stimulation. The fraction of this fluid
which is in contact with the oral and nasal chemical
receptors is continuously replaced due to frequent inhal-
ing and swallowing bursts. These receptors might also
be stimulated by fragrant molecules that have entered
the fetal blood stream. Such molecules may pass from
the blood vessels which irrigate the chemoreceptors [19].
Although often hypothesized, this activation mode has
not yet been demonstrated in the fetus.
The amniotic fluid carries a large number of fragrant
substances [20]. Its composition shows daily variations
depending on fetal micturition and maternal food in-
take. Animal studies have demonstrated that olfactory
substances which have not been metabolized at mater-
nal, placental or fetal levels can be found in the amniotic
fluid [21]. An increase in placental permeability during
gestation might raise the level of this transfer of dietary
odors. It is well-known by obstetricians and midwives
that the amniotic fluid of mothers having ingested spicy
food shortly before delivery smells spicy [22].
2.2.2. Structural development of sensory transducers
Oral chemoreception. Oral chemoreception is both
tacto-chemical via trigeminal nerve and specifically
gustatory through the activation of taste buds. These
buds can be found as early as 12 weeks and are mor-
phologically mature by 13 weeks [23]. They are
displayed all over the oral cavity at first and then con-
centrate and, at birth, remain mainly on the tongue and
on the anterior hard and soft palate [23,24].
Nasal chemoreception. Nasal chemoreception is per-
formed by three systems whose respective contributions
to the olfactory system remain unclear. The main olfac-
tory subsystem, which in aerial conditions detects weak
stimulation, shows adult-like ciliated neuroreceptors by
the 1lth week. The intra-nasal trigeminal nerve endings,
which - - in air - - mostly respond to strong stimulation
including a tactile (the freshness of menthol) or an ir-
ritating component (the prickling sensation of am-
moniac), appear by the 4th week and respond to
stimulation by the 7th week. The third system, named
the accessory olfactive system and composed at the
periphery by the vomeronasal organ, initiates its de-
velopment by 5-8 weeks and reaches its maximum de-
velopment at the central level by the 20th week. For
some embryologists it is considered that, by this time, it
starts to decline at a variable rate depending on individ-
ual patterns [25]. However, recent data indicate that it
subsists in most adults [26] in whom it has been shown
to be activated by specific compounds [27]. The fetal re-
sponsiveness of this organ is still unknown.
3
2.2.3. Evidence of fetal sensory functioning
Oral chemoreception. Behavioral data on fetal gusta-
tion are weak and inconsistent. Injection of a saccharine
solution into the amniotic fluid of chronic hydramnios
gestations led to a reduction of the maternal abdominal
volume that was attributed to ingestion of the fluid by
the fetus [28]. However, spontaneous fluctuations of the
amniotic volume in this syndrome render this conclu-
sion suspect, since two fetuses observed in similar condi-
tions seemed to increase as well as decrease their
swallowing [29]. It should however be noted that intra-
anmiotic injection of a bitter solution can reduce fetal
swallowing [29]. Electrophysiological recordings in the
sheep have established that gustatory receptors are
clearly functional in utero. The responses to various
stimulation are similar for the fetus, the newborn lamb
or the adult sheep [30,31]. They become larger and
stable with gestational age. Although a large interin-
dividual variability was seen, responsiveness to acid and
bitter stimulation seems to be elicitable earlier than to
salty stimulation [23].
Nasal chemoreception. By the third trimester of gesta-
tion all chemosensory systems of the nose seem ready to
be functional: the nostrils have become patent and let
potential stimulation born by the amniotic fluid be in-
haled. At the moment, there is no direct evidence of fetal
olfaction in the human species. However, such responses
have been demonstrated in the 6th month premature
baby and similar performances may be inferred in
fetuses of equivalent gestational age (GA) [20]. They
become stable by 7-8 months GA. Fetal responsiveness
to chemical stimuli has however been demonstrated in
the rat and in the sheep. In the sheep, for example, in-
tranasal injections of odorant components induce im-
portant HR changes in the fetal sheep, while a control
solution has no such effect [32].
2.3. Auditory system
2.3.1. Potential sources of stimulation
The fetal sound environment. The first series of human
intra-abdominal recordings was performed using
microphones covered with rubber membranes which
were inserted (i) in the vagina or the cervix nearest to the
uterus in either pregnant [33-35] or non-pregnant
women [34,36,37], or (ii) inside the anmiotic cavity after
rupture of the membranes during or after delivery
[34,35,38,39]. Except for the acoustic band analysis of
Murooka et al. [35] and Busnel [37], only global mea-
sures were performed in these studies. On the whole,
they described a very noisy womb (72-96 dB SPL, ref.:
20 #Pa) with only very loud external low frequency
sounds being transmitted to the amniotic fluid. The con-
siderable background noise was interpreted as
originating from te maternal cardio-vascular system.
However, some authors recorded significantly lower
4 J.-P. Lecanuet, B. Schaal/European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
sound pressure levels (SPLs between 30 and 50 dB) in
non-pregnant women or after delivery [33,35].
Maternal background noise. In contrast to the findings
from the initial studies, the more recent ones using
hydrophones, adapted to fluid impedance, and narrow
band analysis have indicated that the womb is a relative-
ly quiet place. When the mother is in a calm environ-
ment and when there are no abdominal gurgles which
clearly emerge with high SPLs from the background
noise, the mean SPLs are comparable to those generally
encountered externally [40-43]. The recorded intra-
uterine background noise is a composite of: (a) elec-
tronic noises from the hydrophone and amplifiers, (b)
ambient external noises and (c) various biological ma-
ternal and fetal noises (respiratory, movements, gastro-
intestinal, cardio-vascular, laryngeal); it is mainly com-
posed of low frequencies under 500-700 Hz. Pressure
levels show a regular and significant decrease as fre-
quency rises. Frequency band analyses have
demonstrated that the important global pressure levels
previously obtained were clue to infra-sounds (Benza-
quenet al. [43] and Gagnon et al. [44] measured 85-97
dB at 12.5 Hz) and/or very low frequencies below 50-60
Hz [43,45] for which human absolute auditory
thresholds are very high. Peters et al. [46] clearly showed
that this high energy peak represents resonance from the
buildings in which the recordings were made. Therefore,
contrary to long-held opinion, this high energy does not
have a biological origin.
Low-pitched pulsation recorded at frequencies above
50-60 Hz and under 500-700 Hz, and interpreted as
vascular sounds, were identified either as the maternal
heart-beat [34,35,47], the umbilical artery [42], the
uterine artery [33], or utero-placental blood flow
[40,43,45]. All the recent data suggest that vascular
sounds, occasionally present in the recordings, are not
always present at the same sound pressure level every-
where inside the human amniotic cavity. For instance,
during delivery, Benzaquen et al. [43] were able to rec-
ord maternal cardio-vascular sounds at the fetal neck
level in only two out of 10 mothers and never during
uterine contractions. This was interpreted to mean that
the sounds were of utero-placental - - not maternal - -
origin. When these pulsating noises could be recorded,
their emergence from the background noise was of only
19 dB SPL at 100 Hz and 2 dB SPL at 650 Hz.
Power spectrum analysis shows that when considering
intra-uterine components at or above 100 Hz, various
values are found as a result of different transducers (best
sensitivity in the low or in the high frequencies) and re-
cording sites. Querleu et al. [40,47], after several series
of recordings far from or close to the placenta with dif-
ferent transducers, measured mean SPLs from 65 to 28
dB SPL, the lowest value being obtained far from the
placenta with only 20 dB SPL at 500 Hz and no more
than 10 dB PL at and above 700 Hz; an overall 25 dB
SPL emergence of the maternal heart-beat was found.
The authors suggested that noises from the placenta
probably have a higher masking effect than cardiac
noise. Gagnon et al. [44] with another type of
hydrophone located in a pocket of fluid near the fetal
neck and, therefore, far from the placenta, measured 60
dB SPL at 100 Hz with less than 40 dB above 200 Hz.
Thus, it now seems clear that the contribution of vascu-
lar sounds to the recorded background noise depends on
the location of the transducer.
In utero attenuation of auditory stimuli. The most re-
cent band analysis on the attenuation of airborne broad-
and narrow-band noises and pure tones when emitted in
close vicinity (less than 2 m from the maternal abdomen)
show that there are variations in the in utero SPL in
both the human [48,49] and the ewe [41,50-52]. Some
are systematic and related to the distance between the
source and the transducer when the location of the
transducer is changed in utero. Richards et al. [53] and
Lecanuet et al. [52] found that the intrauterine noise
level in pregnant ewes decreased as the distance from the
sound source increased, although Nyman et al. [48] were
unable to confirm this relationship in human subjects;
Peters et al. [54] recently drew iso-pressure lines inside
the uterus of a dead ewe filled with fluid and
demonstrated that the attenuation of frequencies over
1000 Hz increased from the outside to the center of the
cavity suggesting a 'wrapping around' effect. Others
sources of variation are less clearly defined.
Major results - - most of these obtained in sheep - -
can be summarized as follows:
(1) The pressure levels of sounds at long wavelengths
and low frequencies ( < 300 Hz), were generally compar-
able in and ex utero: in utero measurements showed
some variability with several dB SPL attenuation or
enhancement (at 50 and 63 Hz in the sheep for Peters et
al. [55]) depending on the research teams. When the
wavelength of the frequency is longer than the diameter
of an object reached by this frequency the entire volume
of the object may be set in motion by this frequency
without sound absorption.
(2) According to Peters et al. [55], in utero pressure
loss in the ewe was moderate between 400 and 1000 Hz
and grew by 6.5 dB/octave on average between 1000 and
8000 Hz, thus peaking at 20 dB. Lecanuet et al. [52]
found that this pressure loss started around 300-500 Hz
depending on the distance between the hydrophone and
the abdominal skin of the ewe. In the human, Querleu
et al. [40] reported a similar pressure drop of 20 dB
developed at a rate of 6 dB/octave, while Richards et al.
[49] recorded a maximum attenuation of 10 dB at 4000
Hz. In all recent studies and in both species, maximum
attenuation never exceeded 30-35 dB SPL up to 10 kHz.
(3) A shift tendency has been found in the ewe at
higher frequencies, the in utero pressure increasing and
becoming even higher than ex utero pressure, a phenom-
 J.-P. Lecanuet. B. Schaal/ European Journal of Obstetrics & Gynecologyand Reproductive Biology 68 (1996) 1-23
enon already seen in the measurements of Vince et al.
[50]. Peters et al. [55] observed this reversal from 12 500
Hz onwards and because they used 1/3 octave band
noise stimuli, they found it to be linear. Using sweeping
pure tones, Lecanuet et al. [52] have found such in-
creases as low as 4000 Hz, the frequency values depend-
ing again on the depth of the hydrophone in the sheep.
These increases appeared as a series of pressure peaks of
resonance and anti-resonance probably due to standing
waves caused by reflection of the short waves on the in-
ternal walls of the uterus.
Differentiation of speech from background noise. Data
on voice differentiation and attenuation in utero agree
with the results presented above. Recent acoustical
recordings revealed that the maternal voice as well as ex-
ternal speech located near the mother clearly emerged
from the uterine background noise components over 100
Hz. Recordings performed by Bushel [37] and Querleu
et al. [40] (with an SPL level of 60 dB) have shown that
both the mother's and others' speech: (a) was muffled
and significantly attenuated in the high frequency com-
ponents, (b) had well preserved prosodic characteristics,
and (c) was somewhat intelligible since some phonemes
(up to 30% in Querleu et al. [40]) and words could be
recognized by adults when the recordings were perform-
ed far from the placenta. This is also true of external
voices recorded from the pregnant ewe by Vince et al.
[50,51] and Gerhardt [41]. In a recent work, Griffiths et
al. [56] found that phonemes emitted by a male voice
and recorded in a pregnant ewe had a mean intelligibil-
ity score of 55% (61% at 85 dB, 47% at 75 dB and 41%
at 65 dB) while they had only a 34% mean score when
emitted by a female voice. Compared to external recor-
dings the intelligibility scores were respectively reduced
by 29% and 50%. Analysis of VCV stimuli transmission
showed that voicing information was better transmitted
in utero than place or manner information, that was less
preserved for a female than for a male speaker. In utero
speech, in certain recording conditions, may even be
clearly intelligible in the human [43,57] or the ewe
(Lecanuet et al. [52] at 90 dB SPL).
Human studies of in utero speech transmission per-
formed with a hydrophone near the fetal head during
delivery have all shown that there is a significantly better
transmission of the maternal voice than of the external
voice. Querleu et al. [40] and Benzaquen et al. [43]
measured an overall 20 dB SPL attenuation of external
voices, with no significant difference between male and
female voices. In contrast, there is only an 8 dB SPL at-
tenuation of the maternal voice. Richards et al. [49]
recorded the maternal voice - - which had an external 72
dB SPL level - - 5 dB SPL louder in utero than ex utero.
External voices - - emitted at 90 dB SPL - - suffered
almost no attenuation at all: 2 dB for male voices and
3 dB for female voices; this represents a mean difference
of only 8 dB between the maternal voice and external
5
ones in this experiment, therefore comparable to the 12
dB difference reported in Querleu's study [40]. It is of in-
terest to note that results related to in utero maternal
bleats in the pregnant ewe are similar. Gerhardt [41]
recorded no attenuation in components up to 300 Hz,
while Vince et al. [51] noted several dB SPL enhance-
ment of these frequencies inside the uterus compared to
simultaneous ex-utero recordings; pressure loss started
only at around 1700 Hz.
The higher in utero sound pressure level of the mater-
nal voice compared to the sound pressure level of exter-
nally presented voices spoken at the same level can be
readily explained by the particular mode of transmission
in utero via two different pathways. On the one hand,
the maternal voice is airborne and is transmitted like
any other close external sound and may thus suffer from
the same acoustic modifications. On the other hand, the
maternal voice is internally transmitted via body tissues
and bones. Petitjean's [58] study confirmed the excellent
bone conduction of the fundamental frequency and
higher harmonics through the spine and the pelvic arch.
Sound isolation of the fetus. Transmission of external
pressures to the fetal ear is controlled by two factors that
compose the isolation from the sound environment: (i)
the attenuation due to the transmission to the amniotic
cavity and (ii) the transformation of the in utero
pressures into cochlear displacements. While, as
demonstrated above, the first factor has been quite ex-
tensively described the proportion of the in utero
pressures that reaches the fetal internal ear remains un-
known. This proportion depends on the transduction
mode at fetal head level; it is either directly made
through the external and middle ear fluids or via bone
conduction in the fetal head. For the moment, the
pathways taken by acoustic pressures have not been
defined.
Gerhardt et al. [59] attempted to define the isolation
of the fetal sheep cochlea - - i.e. the attenuation plus the
biological transduction - - by comparing the external
pressure levels necessary to elicit identical cochlear
potentials before and after delivery. Values of this isola-
tion grew from 11 dB at 123 Hz to 45 dB at 2000 Hz.
Abrams et al. [60] concluded that the fetal ear is not pro-
tected from low (< 123 Hz) frequency signals, an impor-
tant finding in view of the fact that low frequency signals
are coded in the fetus by cochlear cells that will later
code high frequencies and thus need to be protected in
the prevention of future auditory deficits. Rubel and
Ryals [61] showed that the cochlear tonotopy (i.e. the
spatial distribution of frequency sensitivity in the
cochlea) changes during maturation.
2.3.2. Structural development of sensory transducers
In the inner ear, the cochlea develops from the
otocyst, a structure appearing around the 28th gesta-
tional day. It starts to curl by the 6th week, reaches its
6 J.-P. Lecanuet, B. Schaal/European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
full morphological development - - measuring 3 mm and
curled into 2 and 1/2 turns - - by the 10th week, and its
final adult size by the 20th week. The organ of Corti,
which bears the auditory receptors, develops within the
cochlea from the 8th week onwards. The first auditory
cells (inner hair cells) and the three rows of outer hair
cells can be seen as differentiated types of cells by the
1lth week. None of them are functional at this age, nor
at the 14th week when the cell positioning on the basilar
membrane has reached its final stage [62].
According to Pujol and Uziel [63], who base their in-
ference on the parallelism in chronology of cochlear de-
velopment in humans and in every studied mammal, the
human cochlea seems functional by the 18-20th week,
while histological studies have shown that the auditory
receptors are not completely mature at this time. The
first cochlear potentials can be recorded in all animal
studies at the same developmental stage. It is by the 20th
week that the efferent innervation of the outer hair cells
takes place, mature synapses being found between the
24th and 28th week [64]. Maturation of inner ear prob-
ably ends during the 8th month with the organization of
afferent and efferent synaptic connections.
At the onset of cochlear functioning, auditory com-
petencies, which have been characterized in animal stud-
ies, are poor. Electrophysiological responses can only be
recorded for medium frequencies (1000-2000 Hz,
depending on the species). Auditory thresholds are high
(around 100 dB); there is no frequency discrimination
and no temporal coding. However, these abilities im-
prove rapidly, and gradually auditory thresholds
decrease, temporal coding begins, frequency sensitivity
widens first in the low frequency range, followed by the
high ones, and finally unit frequency sharpens. The first
cochlear potentials are evoked by mid-frequencies, al-
though the base of cochlea, which usually codes high
frequencies when mature, is the first cochlear zone to
develop [61 ].
It has been thought that residual embryonic mesen-
chyma and amniotic fluid, still present in the external
and middle ear at birth, may impair in utero middle ear
functioning. However, the anatomical studies of
MacLellan et al. [65] and the tympanometric studies of
Keith [66] showed that they do not induce ear drum and
ossicles stiffness. Nevertheless, it can be assumed that
the middle ear is not necessary for fetal audition since
it is adapted to the amplification of acoustic stimuli in
aerial life. Without this amplification, clinical studies
show that there is an average loss of 30 dB from the
aerial environment of the outer ear to the liquid environ-
ment of the cochlea. In utero, since, the outer and mid-
dle ear are filled with amniotic fluid, and since liquids,
tissues and bones have close conducting properties, the
acoustic energy inside the uterine cavity can reach the
cochlear receptors with negligible energy loss, thus, sup-
pressing the need for an amplifying system. Middle ear
transmission might still be possible, however, as pointed
out by Rubel [67], its prenatal functioning is necessarily
different from its postnatal one.
2.3.3. Evidence of fetal sensory functioning
Data obtained in several mammalian species have
brought electrophysiological and neurochemical
demonstrations of prenatal auditory function. In the
human, cardiac and motor responses to several vibro-
acoustic and acoustic stimulation have been studied and
some evoked potential measurements have been per-
formed during labor.
Auditory evoked potentials. Fetal brainstem and cor-
tical auditory evoked potentials have been extensively
studied in utero in the chronically implanted guinea-pig
[68] and sheep [69]. These potentials display the same
characterisics and the same developmental course as
those recorded ex-utero. In the human, they have been
recorded with electrodes placed on the fetus' scalp dur-
ing labor [70-72].
In the premature baby, short, middle and late latency
evoked auditory responses have also been extensively
examined. All three may be recorded, but are not con-
sistently detectable at 24-25 weeks gestational age
(GA). Detectability of major components progressively
increases with age, and is stable by 30-32 weeks
[73-75]. Brainstem responses are consistent and
reproducible, but as previously inferred from animal
studies (see above) - - with very high thresholds (100 dB
SPL) at 25 weeks. Thresholds gradually decrease with
development and by 35 weeks GA are no more than
10-20 dB Hearing Level different from the threshold of
adults. The five principal components showing neural
activation from the cochlear nerve to the inferior col-
liculus are then regularly obtained but are still immature
with regard to peak and inter-peak latencies and
amplitudes.
Neuro-chemical responses. Local cerebral (14-C) 2-
deoxyglucose uptake (2-DG). This method, which
allows investigating fetal brain activity in utero through
cerebral glucose utilization (energy metabolism), has
been used in two animal models, the fetal guinea-pig
[76,77] and the fetal sheep [78]. Pure tones, in guinea-
pigs, and vibro-acoustic stimulation, in sheep, induce a
marked increase in 2-DG uptake in auditory structures:
in the brainstem in the guinea-pig, and in all auditory
structures, including the auditory cortex, in the fetal
sheep. In the guinea-pig, frequency-specific auditory la-
beling has been obtained to loud, external free-field pure
tones up to 20 kHz. The location of the labeling in the
cochlear nucleus and in the inferior colliculus is a func-
tion of the frequency of the tones. The tonotopic organi-
zation of the structures has thus been seen in utero.
Behavioral studies. When obstetricians began in-
vestigations into fetal responsiveness, guided by the
observations made by many pregnant women that their
 J.-P. Lecanuet, B. Schaal/ European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
babies moved when a very loud noise occurred, they
analyzed fetal responses to 'naturalistic' stimuli like
warning horns [79,80] and wood claps [81-83].
Administration mode and structure of stimulation:
In the 1950s, experimenters started utilizing carefully
defined acoustic stimulation, like pure tones and band
noises, emitted through loudspeakers located at various
distances from the maternal abdomen. Later, this air-
borne mode of stimulation was abandoned in favor of
stimulation applied directly on the mother, near the fetal
head, so as to avoid or minimize sound pressure loss.
Two procedures were used:
(a) Stimulation was directly transmitted to the mater-
nal abdomen by an oscillatory source (vibro-acoustic
mode) usually a bone vibrator, a tuning fork, an electric
toothbrush or the Electro-Acoustic Larynx (EAL). The
EALs that were adopted in the 1970s, deliver broad-
band noises at a fundamental frequency of 87 Hz with
multiple harmonics up to 20 000 Hz [84,85]. The surface
of the instrument also vibrated at all frequencies be-
tween 10 Hz and 15 000 Hz. Intrauterine pressure esti-
mation during EAL application has varied between 95
dB [86] to 138 dB [87]. Gagnon et al. [44] measured an
average pressure during active labor of 95 dB SPL which
can be as high as 123 dB.
(b) Stimulation was air-coupled, and in most cases the
loudspeaker (usually part of headphones) was isolated
from the mother's abdomen with a rubber or foam ring.
Vibro-acoustic devices are designed to propagate
sound pressure more efficiently through tissues and
fluids than through air. Impedance mismatches are
therefore avoided. However, such devices may activate
fetal cutaneous receptors which mature very early in de-
velopment [7] and also possibly the sacculus. The latter,
which is part of the vestibular system, matures 2 weeks
earlier than the auditory apparatus [88] and is known to
be activated by loud low frequencies in different species
including the human [89,90].
The air-coupled procedure is likely to result in impor-
tant alteration of stimulus if the loudspeaker is applied
directly to the mother's abdomen. The loudspeaker
membrane is partially blocked thus producing frequency
distortions and high frequency amplification. In con-
trast, when the loudspeaker is coupled with a rubber or
a foam ring, it is the low frequencies that are more likely
to be amplified. Therefore, the conditions produced by
these two procedures are very different from the condi-
tions of fetal auditory activation by external everyday
sounds. This is probably why, in the 1980s, investigators
came back to the use of airborne stimulation by placing
loudspeakers at various distances from the maternal ab-
domen (1 m-10 cm) [45,47,91-96].
Since fetal studies began, various types of stimuli have
been emitted via the different administration modes - -
airborne, air-coupled or vibratory: pure tones, various
bandwidth frequency noises, high-pass filtered or un-
7
filtered pink or white noises, and the EAL stimulation.
Even though the Sound Pressure Levels - - measured
at different ex or in utero sites - - varied across a wide
range of SPLs (from 65 to 123 dB SPL), most studies
were performed at or above 100 dB SPL.
Nature of fetal responses:
It has been repeatedly mentioned before that the
trivial signal of fetal audition perceived by any third tri-
mester pregnant woman, was a fetal startle. Thus, the
first systematic observations were concerned with the re-
cording of motor responses and the concomitant heart
rate changes.
1. Motor responses: Since the earliest observations,
motor responses were classified either as isolated,
strong, and sudden: i.e. startle responses, or as a sustain-
ed increase in fetal activity. Inhibition of ongoing move-
ments [36,80,97,98] and habituation to the stimulus
(cessation or a decrement of responses after repetition of
stimulation) were also described very early [99], and
regularly observed in many subsequent studies
[38,100-102].
In order to detect fetal startles, Peiper and other early
investigators had to rely either on visual or tactile esti-
mation of fetal movement or on mother's perception of
movement. More recent studies have demonstrated - - as
mentioned below - - that mother's perception of move-
ment is only partially reliable [103]. Researchers attemp-
ted objective recordings of maternal abdominal wall,
independently of those evoked by mother's breathing.
Different systems using pressure transducers [82,99,104]
or piezo-electric accelerometers [105] were built to rec-
ord the abdominal changes more precisely.
Analysis of fetal motor responses entered a golden age
with the development of real time ultrasound scanning
systems in the 1960s. A great number of studies produc-
ed startle response estimations by looking at a trans-
verse view of the fetal trunk and lower limbs. This was
either (i) performed on-line by the ultrasonographist
who knew - - and this might bias the observation - -
whether the fetus received a 'true' or a sham stimulation;
and/or by a second observer who looked at the ultra-
sound image on a video screen placed in an adjacent
room to the test room, or (ii) defined a posteriori by
several independent observers on 'blind' videotapes of
trials.
Latency of a specific movement has not often been
computed. Experimenters usually looked for the occur-
rence of any movement before a previously fixed delay.
Of course mean or median latency depends on this
delay. When, this delay lasted several minutes, as in the
case of the non-stress test, latencies for global move-
ments ranging from 6 to 92 s were recorded [106] (aver-
age latency was 64 s when fetuses were in a quiet sleep
state and 24 s in an active sleep state). With a few
seconds delay, recorded iatencies ranged between 1-2 s
[47,86,107], or were less than 5 s [93,108]. Hepper and
 8 J.-P. Lecanuet, R Schaal/European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
Shahidullah [109] found an average latency of 0.34 s
(evoked by a pure tone 250-Hz stimulation given be-
tween 80 and 100 dB) a value close to those recorded in
the newborn studies. Comparison between maternal
perception of response movements and
ultrasonographically detected response movements
showed that between 23 and 29 weeks, the mothers 'feel'
approximately 50% of these movements (the rate of
movements increase from 22% to 94% during this
period) [103]. Over this age, mothers detect 95% of the
movements induced by over 103 dB stimuli according to
Yao et al. [1101.
Local components of the startle response have also
been ultrasonographically analyzed: head rotations
and/or retroflexions, extension/flexion and/or abduc-
tions of upper and lower limbs, hand or mouth opening
[108,111]. Tongue protrusions, cheek movements and
hand-to-face movements, the simultaneously spontane-
ous occurrence of which is rare, have been reported by
Kuhlman et al. [107]. It should be noted that in the very
first study performed using a vibroacoustic stimulus,
Birnholz and Benacerraf [249] observed the eye-blink re-
sponse, a motor activity which is less than easy to detect
on the ultrasound imaging. This response, the most sen-
sitive component of the startle response has an average
latency of 0.031 s, [112] from 33 weeks to normal term
in the premature baby. It occurs in utero in conjunction
with cheek and forehead contraction with an average la-
tency of 0.5 s. Using an electronic analysis procedure of
ultrasonographic B and M imaging modes, Ishige et al.
[113] computed eye-blink and eyeball rotation latencies.
From 29 weeks on, their average latency was 0.099 s.
Looking at leg movements evoked during a 5-s air-
borne 105-110 dB broad band noise, Granier-Deferre et
al. [92] and Lecanuet et al. [95,96] defined three types of
fast movements: (i) a leg flexion or extension, followed
or not by a return to the initial location, (ii) a double
flexion at hip and knee levels ((i) and (ii) were usually
followed by a leg or body translation and rotation) and
(iii) leg movements induced by a global body displace-
ment. Median latencies ranged from 0.73 to 2 s depend-
ing on the acoustical structure of the noise. These values
are far longer than the acoustic startle latencies recorded
in the newborn: from 0.16 to 0.67 s [79,114-117]. How-
ever, it is difficult to assess this parameter, precisely be-
cause the leg was sometimes startling out of the frame,
and these leg movements on average lasted 1.25 s (range,
0.34-3.1 s) whatever the fetal state.
Some very intense acoustical stimuli (> 110 dB) and
most vibroacoustic stimuli induce a long lasting (up to
30 min according to Gelman et al. [118]) increase in the
number of movements compared to the pre-stimulation
period. This increase usually reflects a change in fetal
state, a point that is developed later.
2. Heart rate responses: Mostly phasic Heart Rate
(HR) accelerations, but also sustained HR modifica-
tions, such as tachycardia, or a change in HR variabili-
ty, were described as cardiac responses. Some authors
studied both motor and cardiac responses and showed
that motor response rates were lower than cardiac accel-
eration rates [36].
- - Nature of response as a function of SPL:
Most studies on fetal audition have used loud stimuli.
Two factors influenced the design of these studies. First,
due to the idea that the fetus was sensorially isolated and
to observations of pregnant women that their babies
moved when a very loud noise occurred, it was believed
that last trimester fetuses probably perceived only sud-
den, very loud, sounds. Second, the major clinical con-
cerns, which were antenatal detection of deafness and
diagnosis of fetal well being, required the use of acoustic
stimuli that were easy to deliver and were known to elicit
startle responses (sudden, strong motor responses), easi-
ly recognizable in daily medical practice. Thus, we will
first review major results from the startling stimulation
studies and then describe the promising data obtained
with less intense, non-startling stimuli.
Startnng stimulation:
1. Ontogeny of responses:
(a) Using pure tones stimulation, motor responses were
first detected in vibro-acoustic and air-coupled studies
at 27-28 weeks [97,119] or at around 7 months [36,118].
Cardiac accelerative changes were described as early as
5-6 months [102], 26 weeks [120], 27 weeks [971, 28
weeks [119], or 30 weeks [361. Because of the important
experimental design differences, no precise conclusion
can be drawn concerning the ontogeny of fetal responses
to pure tones. However, a gradual increase in respon-
siveness was observed with gestational age for both
motor responses [36,97,121] and cardiac accelerative
changes [36,80,97,120,121]. According to Sontag and
Wallace [104], cardiac accelerations displayed larger
amplitudes as fetuses get older. By 8 months, motor re-
sponse and accelerative change rates found in most stud-
ies were between 70-90% [36,80,97,120,1211. These
discrepancies may be explained by differences in re-
sponse detection procedures and also because of stimu-
lus characteristics. However, no systematic studies have
been performed to analyze the effect of frequency, inten-
sity or duration of stimulation on the proportion and
characteristics of early fetal responses to pure tones.
(b) Vibro-acoustic studies using broad band noises and
EALs have shown that motor responses, i.e. reliable
stimulus driven movements, were evoked in some fetuses
as early as 24 weeks GA [86,123,124] and in all subjects
at 26 weeks [125], 28 weeks [47,86,107,126] or 30 weeks
GA [108,123,124,127]. According to Leader et al. [123]
only 7% of fetuses responded by 23-24 weeks while
there were 89% by 27-28 weeks. The onset of the re-
sponse occurred earlier in females than in males: 75% of
the 12 females responded by 25-26 weeks, compared to
only 33% of the 15 males. All females responded by the
 J.-P. Lecanuet, B. Schaal / European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
28th week, whereas 80% of the males responded at this
age level. The authors consider this is according to
established neurophysiological data as female infants
mature earlier than males [128].
Very early diffuse motor responses of slow latency
were recorded as early as 20 weeks GA by Shahidullah
and Hepper [129] using a 110-dB broad band noise in an
air-coupled situation. However by 25 weeks, the re-
sponse had become an immediate startle-type one. Ac-
cording to the authors, the development of the outer
hair cells, or some other maturational process occurring
within the auditory system, may contribute to this
change in responsiveness.
- - Two classes of HR responses
Concerning em'diac responses, we have seen that ad-
ministration of a 5-s EAL stimulation induces first an
acceleration followed by a delayed response which con-
sists of an increase in the number of HR accelerations
between 10 and 20 min. Concerning the maturation of
the first response, developmental time course compared
to motor responses was delayed by 2-3 weeks
[122,127,130] similarly to pure tone responses. Kisilev-
sky et al. [125] did not find reliable cardiac accelerations
before 29 weeks. The pattern of this first type of re-
sponse was found to be rather discontinuous 'with a
rather abrupt change from no response to a relatively
mature response between 29 and 31 weeks'. The authors
mention that at 26-28 weeks, 9/12 subjects showed an
average HR deceleration of 2.6 beats/min instead of the
expected HR acceleration. Several maturational ex-
planations are considered and it is noted that this result
suggests an independent control of HR and movement
response (the somato-cardiac effect of the concomitant
movement should evoke an HR acceleration). Accord-
ing to Gagnon et al. [130], the initial HR acceleration
shows an increase in its amplitude between 28 and 30
weeks as well as the appearance of an inverse relation-
ship between the prestimulus baseline and this
amplitude. The authors consider that the rapidity of this
response after stimulation ( < 10 s) indicates that it is
provoked by direct stimulation of the autonomic ner-
vous system, which is functionally mature by 30 weeks
and not a response mediated through catecholamine re-
lease by the adrenal medulla. The delayed cardiac re-
sponse - - an increase in the number and incidence of
gross fetal body movements that could persist up to 1 h
in some fetuses - - is found only after 33 weeks GA. In
approximately 15% of term fetuses there is a l~'ofonnd
tachycardia lasting up to 90 min [111,130,131], 'which
does not correspond to any typical F H R pattern
observed under resting conditions'. In addition, fetal
movements and breathing patterns are also severely al-
tered after 33 weeks. Term fetuses breathe less and more
irregularly following stimulation. Petrikovsky et al.
[ 132] observed that fetal swallowing rate increased from
17% to 42% after a VAS. The same stimulation induced
sustained fetal panting (125 breaths/min one day 117 the
next day) in a 30-week at-risk fetus [133]. As mentioned
above, these modifications reflect a change in fetal state
provoked by the stimulation. According to Visser et al.
[111], a small number of fetuses of healthy pregnant
women at term showed a switch from fetal state 1F
(quiet sleep) to either 2F (active sleep) or 4F (active
wakefulness) following stimulation with the EAL.
Under normal conditions, the human fetus experiences
spontaneous transitions from state 1F to state 2F, and
then, to state 4F.
2. Effects of stimulus characteristics, fetal behavioral
state and risk status:
In near-term fetuses (35-41 weeks GA) as in
newborns, responses evoked with loud vibro-acoustic or
airborne stimuli (over 105 dB SPL) are modulated by
the characteristics of both the stimulus and the fetal
state.
- - Effects of stimulus characteristics
(1) Acoustical structure
The three groups of recent airborne studies mentioned
above demonstrated that broadband noise given at the
same SPL, 110 dB, elicited much higher rates of ac-
celerative changes and motor responses than pure tones
or narrow-band noises. This is in contrast to the air-
coupled and direct vibratory conditions where high pro-
portions of responses were obtained with pure tones. A
probable explanation is that the SPLs reaching the
amniotic fluid are much greater in the latter condition.
(2) Pressure level
As mentioned before, most studies were performed
with loud stimuli (over 100 dB SPL) that induced - -
more or less reliably - - an HR acceleration usually ac-
companied by a motor response. In the airborne mode
of stimulation, Kisilevsky et al. [93] found that the
threshold intensity for a reliable HR acceleration is
somewhere between 100-105 dB. Lecanuet et al. [96]
found that when controlling fetal state, relatively high
percentages of HR accelerative responses were elicited
with octave-band noises presented at 100 dB in a high
variability HR state: 50% at 2000 Hz and 55% at 5000
Hz, with an average amplitude of 18 beats/min for the
two frequencies.
Whatever the stimulation mode, when acoustic pres-
sure level of the stimulus was enhanced, motor and car-
diac response rates increased, as did acceleration
amplitudes [93,110,134]. A 5-dB SPL difference was suf-
ficient to modify fetal responsiveness [93]. This general
increase was observed independently of fetal behavioral
state. However, both cardiac and motor responsiveness
were greater in high HR variability (active sleep) than in
low HR variability (quiet sleep) [95,135].
(3) Frequency/pitch
Contradictory results have been obtained in studies
using pure tones (in air-coupled and vibratory modes of
stimulation), responses rates being higher for high fre-
10 J.-P. Lecanuet, B. Schaal / European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
quency stimulation than for low frequency stimulation
or vice-versa. With broadband noises, given in the air-
borne mode of stimulation, higher pitched sounds in-
duced more responses than lower ones [96]. Low
frequencies, such as a 500-Hz centered noise, induced
very few motor responses. When motor reactions were
induced, the mean amplitude of FHR accelerations was
higher (22 beats/min; ranging from 6 to 48 beats/min)
than when there were no concomitant fetal movements
(12.5 beats/min) thus reflecting a somato-cardiac effect.
- - Effects of fetal behavioral state
Since the work by Nijhuis et al. [136], four behavioral
states have been classically recognized in the near term
fetus: active (2F) and quiet (1 F) sleep, active (4F) and
quiet (3F) wakefulness. In 2F state (active sleep), both
cardiac and motor responsiveness to acoustical stimula-
tion are greater, cardiac accelerations have higher
amplitudes and are more often accompanied with a
motor response than during IF state (quiet sleep)
[95,96,135]. Schmidt et al. [135] also found a greater
reactivity in quiet (3F) and active (4F) wakefulness com-
pared to sleep states. We have seen that when acoustic
stimuli were above 110 dB SPL, or VAS were given, re-
sponse ratios appeared to be no longer modulated by
state; when administered in quiet sleep these stimulation
induced an immediate change to active sleep (state 2F)
or wakefulness with movement (state 4F) [85,93,111],
thus suggesting some disturbing or even stressful effect.
- Effect of risk status
- Non-startling airborne stimulation:
Kisilevsky et al. [137] studying 32- to 34-week fetuses
whose mothers were hospitalized threatened by preterm
delivery, found that when stimulated with a moderately
strong vibro-acoustic signal subjects showed a delay in
the latency of the HR acceleration response and weaker
magnitude of this response (average over l-s intervals)
than non-hospitalized agemates. Since the magnitude of
the hospitalized group was similar to that found in a 29-
to M-week non-hospitalized group the authors suggest
that hospitalized fetuses have a less mature response
than non-hospitalized ones.
After the introduction of antepartum FHR testing,
several investigators using a variety of acoustic stimuli
[138-142] have suggested the use of FHR response to
external acoustic stimulation as an indicator of fetal
health and metabolic status. Clinical use of Fetal Acous-
tic Stimulation (FAS) started with the introduction of
vibroacoustic stimulation with the EAL [143]. Accord-
ing to Gagnon [144], the sensitivity of FAS or VAS used
antenatally to predict intrapartum fetal distress or low
5-min Apgar score has been less than 60% and their pos-
itive predictive value less than 20%. These observations
suggested that VAS may have evoked reactivity in
fetuses with early compromise and raised concerns
about using VAS to discriminate between the healthy
and unhealthy fetuses. In the only randomized controll-
ed trial of VAS for antepartum monitoring [143], no dif-
ference in outcomes was observed between the use of the
VAS and a control group, followed with standard ante-
partum FHR monitoring. Clark et al. [145] tested 2628
women with singleton high-risk pregnancies. Currently
available data obtained from these two studies suggest
that the risk of intrauterine fetal death in the presence
of a FHR response to fetal vibroacoustic stimulatin is
probably not higher than following a spontaneously
reactive nonstress test (1.6 per 1000).
Capitalizing on data obtained in healthy fetuses men-
tioned above, Gagnon [144] recommends that if clini-
cians wish to use antepartum VAS to assess fetal health
and save testing time, criteria for reactivity such as one
FHR acceleration of < 10 beats/min for < 15 s and/or
an increase in FHR baseline of < 10 beats/min for <2
rain following a 3-s stimulus would be adequate criteria
after 30 weeks gestation. Occasionally, more than one
stimulus may be required [143,145,146]. If no FHR re-
sponse is observed, the interpretation of the results
should take into account other factors that could influ-
ence FHR response to VAS. Concerning intrapartum
tests Gagnon [144] recalls that persistently abnormal
FHR patterns in women in labor have a false positive
rate of 50% to predict adverse outcome. Normal FHR
responsiveness to VAS might be falsely reassuring. This
false negative rate also indicates that VAS may occa-
sionally be a stimulus too strong to differentiate the
healthy fetus from the acidotic fetus.
Sounds between 85 and 100 dB SPL ex-utero, do not
induce startle responses or cardiac accelerations, but
evoke moderate heart rate deceleration, unaccompanied
by movement. For example, Leeanuet et al. [96] found
that a 500-Hz octave-band noise emitted at 100 dB
elicited only cardiac deceleration and that the decelera-
tion had the same amplitude in quiet and active sleep
(-10 beats/min). This type of response had been anec-
dotally mentioned by many authors
[36,101,147,148,149]. Some of the decelerative responses
were described as part of biphasic cardiac responses.
Pilot studies confirmed that these cardiac decelerative
responses: (a) could be reliably elicited in quiet sleep
(1 F) fetuses by various types of continuous or rhythmic
airborne stimuli, emitted within this 85-100 dB range ex
utero, and that (b) they quickly habituated to a repeated
stimulus (given every 3-4 s). This made it feasible to ex-
amine the possibility of discriminative auditory
capacities in the 36- to 40-week GA fetus. An habitua-
tion/dishabituation procedure derived from the work of
Clarkson and Berg [150] on speech discrimination in the
awakened neonate was used.
In a first study [151], fetuses which were exposed
every 3.5 s to a pair of syllables ([bal and [bi] or [bi] and
[bad uttered in French by a female speaker, and emitted
at the same pressure level (95 dB) displayed a
decelerative response. Reversing the order of the paired
 J.-P. Lecanuet, R Schaal / European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
syllables after 16 presentations also reliably induced the
same type of response. This response recovery suggested
that the fetus discriminated between the two stimuli.
This discrimination may have been performed on the
basis of an intensity difference between the [ba] and the
[bi], since the equalization of these syllables was done on
the basis of the sound pressure level, not the hearing
level.
In the next study [152], a conservative data analysis
procedure which took into account each subject's pre-
stimulus HR variability was developed. This procedure
defined for each subject: (a) whether the stimulus pre-
sentation and the modification of its acoustic structure
induced a HR change, (b) whether the direction of the
HR change was accelerative or decelerative, and (c)
what its amplitude was. Results obtained by this proce-
dure demonstrated that near-term fetuses exposed to a
short sentence 'Dick a du bon the' uttered by a male
voice (minimum fundamental frequency: Fo = 83 Hz) or
a female voice (minimum Fo = 165 Hz) at the same
hearing level (90-95 dB SPL) and at 3.5-s intervals,
reacted with a high proportion of decelerative responses
(77% to the male voice, 660 to the female voice) within
the first 10 s of stimulation compared to a group of non-
stimulated subjects. After return to a stable HR pattern,
the initial voice (male or female) was either replaced by
the other voice or continued (in a control condition). A
majority (69%) of the experimental subjects, displayed a
HR deceleration to the change, while 43% of the control
subjects displayed a weak amplitude acceleration [152].
The presence of these significant novelty responses
showed that near-term fetuses may perceive a difference
between the voice characteristics of two speakers, at
least when they are highly contrasted for Fo and timbre.
These results cannot be generalized for all female and
male voices or for all utterances. It should be emphasiz-
ed that in this experiment FHR change occurred within
the first seconds of exposure to the novel stimulus, thus
suggesting that only a short speech sample is needed for
the fetal auditory system to detect an acoustically rele-
vant change in speaker. Since the most obvious acoustic
cues for the discrimination are fundamental frequency
and timbre, near-term fetuses in quiet sleep may perform
pitch discrimination as was found during quiet sleep in
the newborn by Alho et al. [154] on the analysis of the
EEG.
1. Fetal responses to musical stimuli:
Almost every pregnant woman has noticed that the
baby she carries seems to react differentially according
to the type of music emitted in the environment. Data
described above suggest that other factors than the type
of music, i.e. its loudness, its pitch, and to a large extent,
the behavioral state of the baby, may control the reac-
tion of the fetus. Thus, the differential average increase
of HR variability measured on a group of 20 subjects ex-
I1
posed to the air-coupled presentation of two distinct se-
quences of classical music by Olds [155] may partly be
due to such effects. A global increase of the number of
HR accelerations and movements is expected in re-
sponse to the presentation of any loud sequence of stim-
ulus, a response observed by Olds to the emission of 5
rain of singing or piano music. An air-coupled presenta-
tion by Woodward [156] of 15 s of a sample of Bach's
organ prelude given at 100 dB induced a high percentage
of HR acceleratory responses (93%) in a High Variabili-
ty state, much more than in a Low Variability state.
Almost all of these responses started within 5 s of pre-
sentation of the stimulation.
Finally, the potential indirect effects of music on the
fetus must be considered: those induced by the maternal
response to this music. This is a very difficult task since
the psychobiological impact of music on an adult
depends not only on the style of the music but also on
the personal history of this subject. Zimmer et al. [157]
gave a 25-min sequence of music to future mothers via
headphones (classical or pop music) and found that the
fetuses of these mothers showed more body movements
and less respiratory movements than during a silent
period. This effect was more significant with the moth-
er's favorite music. Conversely, no modification of fetal
HR was found by Olds [155] during a presentation of
music to the mother through headphones.
2. Fetal responses to maternal speech:
It was mentioned above that, looking for stimuli in-
ducing fetal HR deceleration, we noticed that maternal
speech had this potential. Preliminary unpublished data
suggested that this response was most frequently elicited
in Low HR Variability state (1 F) and when the mother
spoke with a 70 dB Leq level. Recent work by Masakov-
sky and Fifer [158] demonstrated that near-term fetuses
tested in 1F state, showed a HR decrease from baseline
during the last 5 s of a 10-s episode of outloud maternal
speech. Silent or mother whispering episodes did not
evoke a significant HR change.
2. 4. Visual system
2.4.1. Potential sources o f stimulation
In utero visual stimulation appears to be very limited;
however Liley [159] recalls that - - in a dark room - - the
amniotic cavity may be candled with a torch light,
especially in the case of a polyhydramnios.
Measurements performed during rat and guinea-pig ges-
tation have demonstrated that if only 2% of incoming
light was transmitted in utero below 550 nm, this value
increases with wavelength of the signal to reach 10%
around 650 nm [160]. Thus, a limited portion of external
light may reach the human fetal retina when eyelids are
open (this behavior starts at 20 weeks) or through the
eyelids.
12 J.-P. Lecanuet, B. Schaal/ European Journal of Obstetrit~" & Gvnecologyand Reproductive Biology 68 (1996) 1-23
2.4.2. Structural development of sensory transducers
The otic vesicles out of which the retina will stem ap-
pear by 30-32 days of gestation. Major retinal mor-
phogenetic events occur between months 2 and 4 of
gestation. Rods and future cones can be found by the
end of the 3rd month, but the development of
photoreceptor cells is not completed before birth, this
process lasts a few more postnatal months in the
macula.
2.4.3. Evidence of fetal sensor)' functioning
The presumed restricted amount of visual input in
utero has not stimulated the study of responsiveness to
this type of sensory stimulation. A few studies have been
conducted which suggested that: (a) switching on a
bright light bulb in front of the abdomen of a pregnant
woman induced fetal heart rate accelerations [1611; (b)
an increase of fetal motor activity may be obtained after
a sustained exposure to the light (20 min) but not after
a series of 'on and off' switches [162]. However, heart
rate changes induced by a cold light introduced during
an amnioscopy represent more convincing data [163]~
The ontogeny of visual evoked potentials has been
described in the fetal sheep [164]. Stimulation was
delivered by a tiny light source secured close to the eye.
3. Consequences of prenatal sensory experience
Prolonged exposure - - for several weeks and even
months - - of a maturing sensory system to a large vari-
ety of external and/or maternal stimulation may have
several types of effects at either structural, functional or
behavioral levels. Concerning the former levels, prenatal
activation of sensory systems may contribute to the nor-
mal development of peripheral structures and central
connectivity, as well as to uphold their anatomic and
functional integrity during prenatal maturation, lndeed~
if the anatomical macro-organization of neuronal net-
works is genetically designed (neural pathways), more or
less plasticity is possible according to species and sys-
tems, especially regarding micro-organization of neural
networks (development and stabilization of dendritic ar-
borisation and synapogenesis). Incoming sensory stimu-
lation may play a crucial role during this period.
On a more general level, fetal stimulation may also
contribute to the building of perceptual abilities (sensi-
tivity, discrimination) and enable the fetal subject to
process differentially sensory cues that will be relevant
during postnatal life (induction of preferences).
Numerous animal experiments and a few human studies
(see review in [164,165] and [19] or see below)
demonstrate that fetal sensory activation may alter,
through learning, spontaneous pre- and postnatal
responses to auditory and chemosensory stimulation.
They may contribute to the organization of ~he
newborn's preferences for particular stimulation that
will be encountered in the postnatal environment.
Fetal acquisitions can be seen pre- and postnatally.
They can be inferred from a selective responsiveness to
the presentation of a fetal stimulation or from the de-
monstration of a clear preference for this stimulation
when presented in a choice situation.
3.1. Chemosensory stimulation
Animal studies have shown that behavior previously
described as innate was in fact influenced by prenatal
learning. The newborn rat pups show olfactory
preferences or rejections based on prenatal chemosen-
sory learning [166,167]. Rat fetuses exposed to apple fla-
vor, show, when weaned, a drinking preference for an
apple scented beverage than for one scented with maple
syrup [168]. Such a preferential orientation may happen
in natural settings, independently of any artificial
odorisation in the womb. It has been shown that
newborn rats display a preference for the smell of the
amniotic fluid in which they grew [166]. Similar data
have been collected in the newborn sheep and human.
Human neonates presented with the odor of their
amniotic fluid display attraction responses on postnatal
day two [32]. This attraction towards the amniotic odor
is also observed later, on the 4th postnatal day [169].
In the present state of knowledge it is difficult to
assess the duration of fetal learning. Reliable data,
restricted to animal studies, deal with learning processes
(imprinting, aversive learning) to highly biologically rel-
evant stimuli (food, specific vocalizations, maternal
odor) the consequences of which persist without visible
alteration for a long postnatal period. This is the case
for certain maternal olfactory signals the durable attrac-
tiveness of which has been demonstrated without any
post-natally reinforced re-learning. Firstly, young rab-
bits conditioned postnatally to respond positively to
novel odors do not modify their innate preference for
the smell of the maternal nipple pheromone [170]. Fur-
thermore, human newborns, bottle-fed from birth (thus
having no exposure to breast or maternal milk odor)
show, 2 weeks after birth, a clear preference for the smell
of a breast-feeding mother versus the smell of their own
mother's breast [171]. One could legitimately assume
that after birth the large number of novel stimulations,
offering many learning opportunities in conjunction
with disruptions of recognition situations of familiar
prenatal stimuli, might induce a vast reorganization of
prenatal learning and of their retrieval ability which are
due to extinction, generalizations and transfers. The
long-term retention of prenatal chemosensory ex-
periences might be embedded in the anatomical organi-
zation, the olfactory bulb being directly connected to
several paleocortical areas involved in memory and
emotional processing of sensory inputs.
 J.-P. Lecanuet. B. Schaal/ European Journal of Obstetrics & Gynecology and Reproductive Biolog.v 68 (1996) 1-23
3.2. Auditory stimulation
3.2.1. Prenatal effects of sound exposure
Structural and functional effects. Animal studies per-
formed on species in which the auditory function starts
after birth (mouse, rat, gerbil, cat, guinea-pig) have
shown that the afferent input is necessary to establish
and maintain a correct functioning of the auditory sys-
tem and to the partial sound integration in the
brainstem. Bilateral auditory deprivation starting before
or during the period of appearance of cochlear poten-
tials, causes the same anatomical alterations, but to a
lesser extent, than a bilateral destruction of the cochlea:
(i) a reduction in the number and size of the neurons
along the auditory relays of the brainstem acoustic
pathway, (ii) higher electrophysiological auditory
thresholds, and (iii) a reduction in the ability to discrimi-
nate complex rhythmic structures. Monaural depriva-
tion causes neuronal and electrophysiological
alterations affecting mostly ipsilateral structures, deal-
ing with binaural interactions. Several experiments have
shown that sound deprivation would mainly induce a
delay in the development of auditory sensitivity: impair-
ment can be reversible if the deprivation does not extend
to a critical period (see reviews in [172-1751). Such
deficits impair auditory spatial localization [176,177].
On the other hand, prolonged exposure to selectively
enriched sound environments - - which do not induce
any acoustic trauma - - stimulates local dendritic growth
[178], and modifies the reactivity of central acoustic
units [179,180] which seems to facilitate certain
discriminative auditory tasks. Thus, we may assume that
sounds reaching the fetal ear might contribute to the
structural and functional shaping of the auditory
pathway.
Behavioral effects.
Habituation:
1. Motor and cardiac responses in non-pathological
fetuses:
Experiments reported above [151,153] have shown
that repetition at a short interval (every 3-4 s) of a
92-95 dB acoustic stimulus led to the disappearance of
a decelerative cardiac response that had been induced by
the first presentation of this stimulus, thus indicating an
habituation to this stimulus. Due to their interest in the
fetal diagnosis of potential neural defects, a large num-
ber of studies have been - - and are still - - performed to
analyze fetal habituation to loud stimuli. These studies
indicated that the number of stimulus presentations re-
quired to obtain habituation depends on (a) the type of
observed response (motor or cardic), (b) the defined
habituation criteria (i.e. the number of trials inducing no
response, and the use or not of a dishabituation stimu-
lus), (c) the characteristics of the stimulus (spectral orga-
nization and duration, inter-stimulus time interval), and
(d) the fetal behavioral state.
13
With an airborne auditory stimulation, given at or
lower than 110 dB SPL ex utero, local and/or global
components of the startle response significantly decreas-
ed or disappeared after only 2 - 4 presentations
[79,80,94,97,105]. As in the premature baby or the term
newborn, the fetal cardiac response is slower to
habituate than the motor response. Significant reduc-
tion or disappearance of this response is obtained after
2-7 presentations [94,95,149]. The amplitude of the car-
diac acceleration also diminishes after a few repetitions
of the stimuli [95,100,181]. Using a classical habitua-
tion/dishabituation procedure, Kisilevsky and Muir [94]
have obtained a significant decrement of both cardiac
accelerative and movement responses to a complex
noise, given at 110 dB SPL, followed by a recovery of
these responses to a novel stimulus, a vibro-acoustic
one. Fetal state interferes with habituation, this process
being faster during quiet sleep state than during active
sleep state [95]. More recently, Hepper and Shahidullah
[109] found prenatal habituation of the motor response
to sine waves signals with a frequency of either 250 or
500 Hz and a sound pressure level individually defined
for each fetus.
When applying vibro-acoustic stimulation, motor re-
sponse rate decrement is much slower than with air-
borne auditory stimulation. It takes at least 6-40
presentations to occur depending on fetal age, fetal con-
dition and habituation criteria [123,182] (10-50 trials);
[107,183] (blink startle response); [184] (16-18 trials);
[107,185,186]. Among the 15 subjects on their 36th week
of gestation tested on two successive days in the Leader
et al. [123] study, 14 required fewer stimuli for habitua-
tion on day two. Infants tested after intervals of 3-4
days showed no consistent habituation pattern. The
authors concluded that this seems to indicate some evi-
dence of fetal memory that lasts for 24 h and not for 72
The authors did not notice any effect of fetal state.
Motor habituation becomes easier to establish as ges-
rational age increases: with a 12 stimulation habituation
criteria, 31-week fetuses needed on average 10.3 stimula-
tion to habituate and 40-week fetuses only 6.2 [107]. Ac-
cording to Groome et al. [187] who replicated this study
from 28 weeks onwards and coded the strength of motor
responses, there was no change whatever with age of the
subjects but the decrease of the strength with stimula-
tion was faster after 32 weeks than before this age.
Concerning HR responses, Leader et al. [188] tested
habituation to three 5-s EAL stimulations. Stimulation
two and three were given only when the HR rate had
returned to the baseline for 2 min. The HR response was
defined as the HR level 1 min after stimulation. There
was a significant decrease in the response between the
first and second stimuli as well as between the second
an third stimuli. The mean time for the fetal heart rate
to return to its baseline after the first stimulus was 5.8
min (range, 0.5-15 min), after the second stimulus 4.49
14 J.-P. Lecanuet, B. Schaal / European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
rain (range, 0.5-18 min), and after the third stimulus
3.13 rain (range, 0.5-10 min). These results indicate that
the use of VAS in this study did not induce the sustained
and severe tachycardia (as well as the excessive move-
ments) reported by Visser et al. [111 ] and Gagnon et al.
[130]. Indeed, comparing the effect of the toothbrush
used in their 1982 studies with the effect of a Cor-
ometrics acoustic stimulator and a sham stimulation,
Leader [191] found that 'although there were some
changes in fetal state, these were short-lived, and fetuses
who were regarded to have changed to state 4 reverted
back to either state 1 or 2 before the next stimulus was
due'. The authors did not observe the atypical patterns
nor the tachyeardias described as frequent by Visser et
al. [1111. The difference in findings between the studies
is attributed to the intensity and frequency of the VAS.
This, to our opinion, seems unlikely since most VAS
(not electric toothbrush) have similar large frequency
spectra and close mechanical devices. While poorly
plausible, the differences between results might be due
to the fact that (i) the VAS was not placed at the same
location: both experimenters stimulate at fetal head
level, but Abrams [190] found that intra-uterine pres-
sure transmitted from a VAS falls rapidly as distance
from the stimulation site increases; (ii) pressure exerted
by the experimenter with the VAS was different. Leader
[1911 supports his conclusion on the harmless effect of
the VAS with the demonstration by Fisk et al. [192] that
this stimulation is not associated with a rise in adrena-
line or noradrenaline, and the absence of postnatal ef-
fects of this stimulation on auditory functioning [193] or
on infant development [48].
Goldkrand and Litvak [194] also demonstrated HR
response habituation of 28-43 weeks GA fetuses to 20
stimulations of 1 s each given every minute with a VAS.
Kisilevsky and Muir [94] did not observe any statistical-
ly significant FHR accelerative response decline after
eight VAS trials, but only a trend in that direction.
2. Effects of various contextual events on auditory
habituation:
(1) Cigarette smoking and drugs
Leader [195] found that 10 fetuses tested with a VAS
less than an hour and a half after their mother had a
cigarette had an abnormal habituation pattern ( < 9 or
> 50 stimuli) compared to the one they showed 3 - 4 days
before (10-50 stimuli). Other subjects, whose mother
smoked 40 cigarettes a day required 6 h before fetal
habituation returned to normal pattern. Hepper and
Shahidullah [109] showed that fetuses whose mothers
smoke required a greater intensity of stimulus to evoke
a response compared to those whose mothers did not
smoke.
In addition, Leader [1911 compared the evolution of
the habituation rate of a group of fetuses of non-smoker
mothers tested three times (the second time 30 min after
the first, the third time 20 min after the second) and the
rate of a group of fetuses of smoking mothers who had
refrained from smoking for 6 h but had smoked two
cigarettes at the end of the second trial. There was a pro-
gressive decrease in the number of stimuli required for
habituation after the third trial in the non-smokers
group. Smokers fetuses took significantly longer to
habituate than the non-smokers.
The same research group compared habituation rates
on a control group (no-drug) and a group of fetuses
whose mothers had taken 30 mg of phenobarbitone
every 8 h for 3 days. While the two groups did not differ
on a habituation test given day one, before the barbitu-
rate ingestion, only three fetuses out of nine in the drug
group had a normal habituation pattern on a test given
on day 4-5. When retested after stopping the sedatives,
their habituation pattern had returned to normal.
Kuhlman et al. [107] found that drug addicted mother
fetuses habituate slower than those of mothers who do
not take drugs.
(2) Alteration in inspired maternal oxygen
Leader and Baillie [1961 analyzed the effect on fetal
habituation to their vibro-acoustic stimulus of breathing
by the mother of only 12% oxygen during the test. This
is equivalent to living at 13 000 feet above sea level and
reduces the maternal Pao2 from 99 mmHg to 44 mmHg.
The arterial saturation, however, only falls to 86%. Two
counterbalanced experimental groups had the 12% oxy-
gen breathing either on a first or on a second test given
the next day. In both cases, only one fetus out of eight
and 10 showed a normal habituation pattern under this
maternal breathing situation, while all fetuses in the
experimental group having the 12% oxygen on day two,
and 7 out of 8 in the group having the limited oxygen
on day 1 showed a normal habituation pattern.
3. Fetal pathology:
Of two cases of Down syndrome tested for habituation
to a pure tone stimulus by Hepper and Shahidullah
[1091, one failed to habituate and the other took longer
to habituate than control subjects. One of the two who
failed to show any change in its motor response latency
died shortly after birth, although there was no detec-
table difference between the two antenatlly.
In the VAS study by Leader et al. [183] giving three
stimulation and measuring HR change, at risk fetuses
(suspected of intrauterine retardation or of mothers
showing hypertension) had not only an initial response
significantly smaller than normal fetuses but there was
no habituation of the response on trial two and three.
Coaditioai~:
Two controversial attempts at establishing a classical
conditioning have been conducted [82,831. A non-
startling conditional stimulus (a low frequency vibra-
tion) was repeatedly presented before an unconditional
startling sound stimulus until it was able to evoke this
startle response. Apparently, such a conditioning would
have been erased and reinstated after a 3-week delay.
 J.-P. Lecanuet, B. Schaal/ European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
More recently Feijoo [197] claimed to have associated
the musical theme of Peter and the Wolf by Prokofiev
(given at 60 dB SPL) with a state of deep maternal relax-
ation (presented as an unconditional stimulus inducing
fetal movements) several times a week during the 6th,
7th and 8th pregnancy months. When tested on the 37th
week, trained fetuses responded immediately with move-
ments to the presentation of the musical theme, while
non-exposed fetuses moved only 6-10 rain later.
Backwards presentation of the sequence did not have
any effect on trained subjects.
3.2.2. Postnatal effects of sound exposure
Prenatal auditory experience may result in general
and/or specific learning, the effects of which are seen in
various postnatal situations. Familiar stimuli or classes
of stimuli may - - more or less selectively - - soothe the
crying newborn or elicit orienting responses during quiet
states. Stimuli may loose their avoidance properties
after the baby has been exposed to them during the fetal
life. More convincingly, familiar stimuli or classes of
stimuli can be preferred to unfamiliar ones in choice test
situations (e.g. the non-nutritive high amplitude
sucking).
Soothing and orientation responses.
Maternal heart-beat and other endogenous sounds:
Salk [198,199] first found that newborn babies daily
exposed to the sound of an adult heartbeat emitted at 72
beats/rain - - a sound presumed to be familiar from the
earliest fetal period - - were soothed by this sound, slept
sooner and gained weight more rapidly than non-
stimulated babies. Salk's work was followed by a series
of investigations on the effects of maternally-generated
internal noises. Initially, these studies were restricted to
an examination of the soothing effect of maternal car-
diac noises on the neonate. Results have not been con-
clusive, some describing a soothing effect which others
did not confirm [35,146,200-209]. This is probably due
to differences in experimental design, such as the use of
different types of stimuli, different observation timings
(short-term or long-term).
Murooka [35] comparing various stimuli, including
recordings of the intrauterine background noise (i.e.
recorded close to the placenta and thus including loud
maternal cardio-vascular components; cf. the discussion
on the acoustic structure of internal sounds above) con-
eluded that any noise having an acoustical structure
similar to that noise - - and not only this very stimulus
- - had a short-term pacifying effect. This effect has been
confirmed by Kato et al. [203], and by Asada et al. [210]
who recorded heart rate and respiration rate modifica-
tion in crying babies. Yoshida et al. [211] report a
similar effect on irritable babies, lasting at least for the
first 7 postnatal days. Yoshida and Chiba [212] showed
that the intra-uterine noise emitted at 75 dB lowered the
fundamental frequency (Fo) of crying and elicited posi-
15
tive facial mimics. Using a non-nutritive sucking choice
procedure, DeCasper and Sigafoos [213] demonstrated
that the heart beat sound used by Murooka et al. [35]
had a reinforcing value for 3-day-old babies.
Speech sounds and musical episodes:
It has been mentioned above that speech sounds,
especially those emitted by the maternal voice, were not
masked by the intrauterine background noise. The pro-
longed exposure of the human fetus to such stimuli may
thus have postnatal effects. Natural or synthetic speech
sounds seem particularly attractive to the newborn who
shows transient decelerative responses to the onset of
their presentation [214,215], an effect that may however
be induced by many other auditory low-pitched,
moderately intense, stimuli [216,217]. Many studies con-
ducted during the last 25 years have suggested that
newborns process speech stimuli in a specific way dif-
ferent from other auditory stimuli (see review in Aslin et
al. [218]). This is usually seen as a consequence of an in-
herited human sensitivity to linguistic sounds [219] more
than the effect of a prenatal exposure to speech sounds.
However, these explanations are not mutually exclusive.
The particular attractiveness of the mother's voice on
<2-week-old neonates has been described by several
authors [220-223]. The explanation accounting for this
phenomenon could be postnatal association of this voice
with positive reinforcers rather than prenatal learning.
However, conflicting evidence is presented below.
Concerning musical sequence, Feijoo [197] in the de-
livery room, and Hepper [224] on 4- to 5-day-old babies,
observed that infants were significantly soothed and at-
tentive to musical sequences that their mothers listened
daily during the last 3 months of pregnancy. Feijoo
delivered the bassoon part of Prokofiev's 'Peter and the
Wolf'; in Hepper's study the target stimulation was the
musical theme of the mothers' favourite British TV sit-
com 'Neighbors'.
Long-term habituation to startling stimuli. Prenatal
learning is suggested by two studies of long-term
habituation. Human and guinea-pig neonates are
significantly less disturbed by a startling sound if they
have been repeatedly exposed to it prenatally. The long-
er the prenatal exposure of human neonates - - living in
the Osaka airport neighborhood - - to airplane noises,
the better they slept compared to babies whose mothers
had lived in the area of the airport for shorter times dur-
ing pregnancy [225,226]. In the same line, neonate
guinea-pigs were less responsive (no significant heart-
rate change) to the vocalization of a Bantam hen than
control animals, who had not been exposed to this
sound during gestation [227].
Evidence for auditory preferences.
For the maternal voice:
Concerning maternal voice, studies performed with 2-
to 4-day-old neonates (using a selective Inter Bursts (of
sucks) Interval (IBI) duration reinforcement procedure
16 J.-P. Lecanuet, B Schaal ,European ,/ouretat ot ",Phstvtric~ & G~m'~tw~ev and Reprtnlucltve Btv/.t{~ 06 (1996i I-2.¢
of the non-nutritive sucking) demonstrated that ~ht-
mother's voice was not only attractive to newborns as
mentioned above, but was also preferred to another fe.
male's voice [228,229]. The possibility of a very iast
postnatal acquisition was again argued. The a u t h o r
then compared the preference between airborne version~
of these voices to their 'intra-uterine'. low-pass filtered
versions. No particular preference was evidenced b,.
Spence and DeCasper [230] (while the newborns di<i
prefer an airborne version of another woman's voice
this was considered to be a demonstration of a prenata!
contribution to the neonates' general preference tT~r ~he
mother's voice). Finally, Fifer and Moon [2311 and
Moon and Fifer [232], using a modified version o~ ~hc
'intra-uterine' mother's voice (either mixed or not wilt,
maternal cardiovascular sounds), found that newborn~
preferred an 'intra-uterine' form of their motheffs vo~c~'
over an airborne version. In addition, DeCasper ~md
Prescott [233] found that 2-day-old babies did not prefer
their father's voice to another male's voice even afte,,
4-10 h of postnatal contact with lheir father thi:
postnatal contact was thus insufficient to induce a prefl
erence to this voice. Together, these results suggest ~h,,
the absence of a preference for the father's vmce is prob
ably due to lesser prenatal experience with the father',
voice than with the mother's voice.
Prenatal familiarisation with the maternal voice ma',
explain why Hepper et al. [234] found that newborn~
discriminate normally-intoned speech from 'mothere~
intoned speech (i.e. with exaggerated contours l only fo~
the maternal voice. Subjects discriminated maternal
voice from a strange female voice, however
For a speech sequence:
DeCasper and Spence [235] showed (using the non
nutritive IBI contingent sucking procedure) that 2- l,~ 3
day-old newborns preferred hearing a story their mother-
had read out loud during 6 weeks before birth than a
story that they had never heard. Since no difference ~;_~
found during testing if the story was read by the mother
or another woman's voice, prenatal learning of some ac
oustic features of the story, probably prosodic, is sug-
gested.
For musical sequences:
Using the non-nutritive sucking procedure. Pannct,m
[236] showed that newborns whose mothers had bee.
singing a melody - - using the syllable 'la' instead of the
words of the song - - changed their pattern of sucking
in order to turn on a recording of this melody mort'
often than the recording of an unfamiliar melody; both
melodies contained the same segmental information (i.e
the syllable 'la') and the same individual notes, but the
temporal order, duration and relative number of ti~,:
notes were different in each melody. Woodward l! 561
exposed fetuses from the 34th weeks GA onwards eithc~
to a sequence of classical music or to a sequence of iaz/
music. With a different sucking procedure ti e r~rem,rat
iy presenteO music being contingent to a sucking pause
tan IBI) and novel music being contingent to the onset
ot a burst of sucks in one test condition and vice versa
m another condition), she found that newborns
lengthened the pauses Ireinforced by the 'familiar"
musict and had a smaller number of bursts in the second
part of a 10-min test than in a silent pre-test period in
the firsl codition type of test.
~'or a speech sequence sung by the mother:
tn an experiment performed by Satt [237] with the
DeCasper's non-nutritive sucking test 3 days after birth,
babies had to choose between two recorded lullabies,
both recorded by their mother. During the end of their
fetal lile they had been repeatedly exposed to one of the
iutiabies for which they showed a preference.
For the maternal language:
h~ the tollowing studies, the neonates had some
posmatal experience with the maternal language before
they were tested, either for a specific preference for this
language or for their capacity to discriminate between
the maternal and another language. Using a non-
nutritive sucking choice procedure, with both Spanish-
and English-speaking women. Moon et al. [238]
,',~'mo~sirated that 2-day-old newborns preferred their
mother's language to the other one. Demonstration of a
~,~elerence for the mother's language at such an early
age favors an interpretation of the data of Mehler et al.
{239,2401 in terms of prenatal familiarisation. In these
last studies, 4-day-old babies discriminated between two
languages (French/Russian or English/Italian), one of
which being the mother's language. Moreover, babies
born from French speaking mothers showed a higher
average sucking rate during the habituation phase when
ihe speech emitted during this period was French than
when it was Russian, both languages being spoken by
the same bilingual woman. Such a response persisted
when babies were exposed to low-pass (<400 Hz)
filtered versions of the two languages which kept only
prosodic cues of the spoken sentences. In addition,
babies born from mothers speaking neither French nor
R ussian were unable to discriminate between those two
languages as if the absence of any familiar prosodic cue
rendered the perception of differences impossible. Thus,
such data may reflect either prenatal familiarisation to
specific language, augmented by 3 - 4 days of postnatal
exposure to this language, or fast learning processes
occurring during this neonatal period.
4. Conclusion
Human fetuses are, to a certain extent, able to
memorize certain sensory properties (e.g. within the
auditory and chemosensory modalities) of their environ-
ment. How does this ability work, especially considering
lhat the fetuses spend much of their time in sleep states?
Despite the fact that they have only very short periods
 J.-P. Lecanuet, B. Schaal / European Journal of Obstetrics & Gynecology and Reproductive Biology 68 (1996) 1-23
of wakefulness and that their brain is not mature enough
to integrate sensory experiences, several experiments
suggest that this does not prevent pre- and perinatal
learning. Experiments on the learning abilities of
cerebrolesioned animals and human neonates
demonstrate that remaining infra-cortical structures
may support considerable elementary learning ability
[241,242]. Similar evidence has been provided for
anaesthetized adult animals [243]. Moreover, one may
recall that memory for events does not develop only as
a consequence of conscious suprathreshold perceptions,
but also after various 'subconscious', infrathreshold
stimulation. It has thus been demonstrated on human
adults that an odor delivered below the detection
threshold (not consciously perceptible) in systematic
conjunction with a stressful situation, may elicit nega-
tive attitudes and responses during subsequent en-
counters [2441.
Extending Maurer and Maurer hypotheses [245] con-
cerning the human newborn we confront a very peculiar
representation of fetal perception. According to these
authors the newborn (and thus the near-term fetus)
would be continuously opened to sensory experience - -
even during sleep episodes. Full consciousness, defined
as resulting from the interaction between several brain
levels, would gradually develop during brain matura-
tion. Sensory perceptions may be first organized follow-
ing 'amodal' processes, introducing babies in a
synaesthetic world: they might 'taste' the voice of the
mother, 'smell' the touch of her hand, 'listen' to
odorous, etc. The polysensorial world of the adult may
be simplified into a monosensory experience. Studies
performed on newborn rats by Spear and Molina [246]
bring some experimental support to this hypothesis.
A more classical point of view regarding con-
sciousness considers, along with Kouchner and Tassin
[247], that the poor development of modulatory cortical
neurons and the very limited development of associative
intra- and inter-hemispheric pathways, do not allow the
conscious processing of sensory inputs. Consequently,
stored memories or more carefully stated acquisitions
performed during the very first years of life (including
the fetal period) cannot be voluntarily retrieved since
they had been stored according to a processing mode
that is not directly compatible with the functioning of
the aroused child or adult brain. This does not lead to
consider that early learning experiences do not retain
their potential control on awakened behaviors, but only
that the information stored cannot be retrieved directly
in conscious states.
The corpus of fetal sensory research presented above
may have important clinical impact. Indeed, the above
survey of the relative literature has demonstrated that
the clinical concern has been central in this research.
Almost all studies of fetal responses to vibro-acoustic
stimulation have been conducted in quest of a fast, prac-
17
tical and reliable diagnostic tool for fetal hypoxia. More
than 80 papers have been published and the practice of
the EAL stimulation examination has developed
especially in the USA. Gagnon's recommendations [144]
about the use of VAS have been mentioned above.
Cyclic changes in behavioral state are the major re-
striction to the systematic reliability of analysis of re-
sponsiveness to sensory stimulation as a diagnosis tool.
Firstly, responsiveness of non-pathological fetuses as a
function of state is not well-defined. Secondly, its study
shows that there is a considerable interindividual
variability (Lecanuet et al., unpublished data). Selecting
a more sensitive dependent variable than HR changes
and startle response could renew current perspectives on
the predictive value of sensory responsiveness. A pro-
mising line of research seems to be the global computer-
ized analysis of the succession of behavioral states of the
fetus. Alteration of duration and structure of spontane-
ous transitions between states has indeed been found to
correlate with unfavorable outcomes [248].
Acknowledgement
The authors wish to thank C. Granier-Deferre and
M.-C. Busnel for their contribution to previous elabora-
tion of several parts of this manuscript and A.-Y. Jac-
quet for her very helpful support in the preparation of
the reference list.
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