Persistence of fetal memory into neonatal life
, M.N. SUAREZ1
, B. PEREZ-PIN˜ ERO1
, H. ARMAS1
E. DOMENECH1 & J.L. BARTHA2
Departments of Obstetrics Gynecology and Paediatrics, University Hospital of the Canary Islands, Tenerife, 2
Obstetrics Gynecology and Paediatrics, University Hospital ‘‘Puerta del Mar’’, Ca´diz, Spain
Objectives. To test the hypothesis that fetal memory persists into the neonatal period. Study design. Forty-one newborns that
had been repeatedly stimulated by using fetal vibroacoustic stimulation were compared with 31 controls. The same
vibroacoustic stimulator was used for both fetal and neonatal stimulation tests. For the neonatal test the stimulus was
applied against the mastoid of the newborn with the interposition of a specifically designed solid liquid interface to simulate
intrauterine conditions. Student’s t-test was used. Results. Neonatal habituation rate (the number of consecutive stimuli
applied before a baby stopped responding) was significantly higher in those newborns who had not participate in the fetal
habituation study (7.09/5.4 stimuli) than in those who had (4.19/4.1 stimuli), p/0.01. Conclusions. Newborns who were
stimulated in utero habituated earlier than those who had not previously experienced the stimulation. These results suggest
that fetal memory persists into neonatal life.
Key words: Fetal habituation, fetal learning, fetal memory, vibroacoustic stimulation, fetal behavior
Habituation is a decrease in responsiveness to a
stimulus when that stimulus is presented repeatedly
or for a prolonged time (1). This process is a basic
form of learning and a normal pattern may be one
indication of intact central nervous system function
Fetal habituation to repeated vibroacoustic stimuli
has been used to study fetal memory (3) and it was
concluded that fetuses were able to learn, had a
short-term memory of at least 10 min, and a longterm memory of at least 24 h.
Little attention has been paid to the possible
functions of fetal memory. It has been proposed
that it can be involved in recognition of and attachment to the mother, which may influence promotion
of breastfeeding and language acquisition (4). Moreover, potentially fetal learning and memory may have
a clinical interest if they could be positively influenced.
In spite of these potential benefits, there are only a
few studies focusing on the persistence of fetal
memory into neonatal life (5) and the vast majority
of them did not use an adequate methodology to test
this hypothesis. One of the main methodological
problems of studying fetal learning during the
postnatal period is finding a fetal stimulus that can
be reproduced postnatally, thus able to be remembered by the newborn.
We have developed a neonatal mechanism that
reproduces fetal vibroacoustic stimulation and we
have used that system to test the hypothesis that fetal
memory persists into the neonatal period. This was
the aim of the present study.
Subjects and methods
Forty-one pregnant women who attended the antenatal clinic between September 2001 and August
2002 were studied. The inclusion criteria were as
follows: healthy single pregnancies with absence of
both medical and obstetric disorders, no toxic
habits, cephalic presentation, gestational age between 38 and 40 weeks, and normal fetal growth
assessed by ultrasound.
Correspondence: N.L. Gonzalez Gonzalez, Avda de la Universidad no. 27, 38208 La Laguna, Tenerife, Canary Islands, Spain. E-mail: email@example.com
Acta Obstetricia et Gynecologica. 2006; 85: 1160 1164
(Received 18 April 2006; accepted 5 June 2006)
ISSN 0001-6349 print/ISSN 1600-0412 online # 2006 Taylor & Francis
Maternal weight was 67.69/7.2 kg, maternal
height 162.49/5.7 cm, ultrasound-assessed maternal
abdominal adiposity 16.09/6.1 mm, and gestational
age at the study 39.59/0.3 weeks. Amniotic fluid
index was normal in all cases.
The study was approved by the Local Ethical
Committee and all women gave their written consent
form for the study.
After checking amniotic fluid index, fetal presentation, fetal growth, and maternal adiposity, the
ultrasound probe was placed to observe totally or
partially the fetal face, the upper extremities, and the
upper part of fetal trunk on the same view. In all
cases fetal movements and fetal heart rate (FHR)
were monitored (HP 8041 A) at the same time until
the registered pattern corresponded to a fetal active
state (F2). Then an ultrasound observation was
started and after checking the fetus really was in
active state for longer than 10 min, the study was
initiated. The fetuses were stimulated by using an
artificial larynx as a fetal vibroacoustic stimulator
(calibration made by the manufacturer by checking a
sound level 85 110 dB and audible sound 100
9,000 Hz a meter away from the sound transmitter;
‘‘SERVOX INTON’’, Servox Medizintechnik, Merheim).
This stimulus was repeatedly applied to the
maternal abdomen above the fetal head for a period
of 1 s every minute till a maximum of 24 stimuli.
A general movement of the fetal trunk, the upper
extremities, the head or the eyes starting in the first
second post-stimulus was considered as a positive
response. If the fetus was moving before stimulation,
then a change in the pattern of the previous movements within 1 s after the application of the stimulus
was considered as a positive response. Some fetuses
remained very active after stimulation but no cases
required prolonging the interval between stimuli for
longer than 3 min to evaluate the reflex response as it
was always possible to find an interval to evaluate the
response to a new stimulus.
Habituation was defined as the lack of response to
four consecutive stimuli. Habituation rate was defined as the number of consecutive stimuli applied
before a fetus stopped responding.
Habituation tests were repeated every 48 72 h
until delivery. Eighteen fetuses undertook three
habituation tests, 14 had two tests, and in the
remaining 9 only one test was possible before
All habituation tests were done in the same room
by the same operator between 9:00 and 13:00 in the
morning. Neonatal habituation was compared between the 41 neonates who had undergone fetal
habituation tests and a control group composed of
41 newborns who had not participated in the
fetal habituation study and who had not received any
kind of prenatal vibroacoustic stimulation test. This
group was selected by taking the consecutive healthy
newborn after one of the babies participating in the
fetal habituation study was born. Inclusion criteria
for the control group were healthy singleton pregnancy at term and a birth weight between 2,500 and
4,000 g. Ten neonates of the control group were
further excluded from the study due to loss of
follow-up (mothers first accepted but subsequently
decided to resign from the study). There were no
statistically significant differences in gestational age
at delivery, analgesia in labor, mode of delivery,
Apgar scores, and umbilical pH between the studied
All neonatal habituation tests were done by the
same observer who was blinded to the studied groups.
Neonatal habituation assessment took place
within 1 2 days after delivery before an otoacoustic
emission test was performed. A normal result of this
test demonstrates the integrity of the audit system
and it has been implemented in our hospital as a
universal newborn hearing-screening program. For
the habituation test the newborns were placed into a
soundproof cot in a quiet room, until a maximum of
60 min after a feed between 10 and 12 in the
All babies were observed for 10 min and the
operator waited until the newborn was quiet (neither
crying nor having intense general movements). Then
the same vibroacoustic stimulator that had been
used for the fetal habituation study was applied
against the mastoid of the newborn with the interposition of a solid liquid interface composed of
muscular animal tissue (2 cm thick) plus a plastic
bag of 50 ml of warm saline in order to simulate the
intrauterine conditions by which the stimulus
reached the fetus.
Newborn stimulation was done using the same
protocol as used in the fetal study and applying the
same criteria to define a positive response, habituation, and habituation rate.
Sample size was calculated by using previously
reported data (6 8). Statistical analyses were performed by SPSS 11.0.1. (SPSS Inc Corp, Chicago,
IL, USA). Distributions were checked by histograms
and the Kolmogorov Smirnov test. Results are
presented as mean and SD and qualitative variables
as number and percentage. Groups were compared
using an unpaired Student’s t-test. Comparisons
between the first two measurements of habituation
were made by using the paired Student’s t-test.
When available (n/18), comparisons among the
three measurements of habituation were made by
Persistence of fetal memory into neonatal life 1161
using the ANOVA test. Proportions were compared
by using the x2
-test. For correlations, Spearman’s
correlation coefficient was used. The significance
level was previously set at the 95% level (p/0.05).
All the fetuses showed positive responses to vibroacoustic stimulation. Thirty-nine of the 41 stimulated
fetuses in the first test (95.1%), 30 of those 32 who
undertook the second one (93.7%), and the all the
18 fetuses who received the third test (100%)
habituated (Table I). The two fetuses who did not
habituate during the first test were the same who did
not do it during the second one. One of them was
born before having a third procedure. The other one
underwent a third stimulation test and habituated
after receiving the maximum number of stimuli.
The habituation rate was 7.09/4.6 stimuli. When
two procedures were performed (n/32), the habituation rate was significantly lower in the second one
(Table II). The habituation rate was even lower in the
third one but this could be only studied in those
fetuses who underwent three tests (n/18) and the
differences were only of borderline significance (p/
0.1), probably due to the small sample size (Table II).
The percentage of newborns who showed a
positive response to vibroacoustic stimulation was
similar in both of the studied groups: n/35 (85.3%)
versus n/26 (83.8%) for the studied and the control
groups respectively, p/0.86. The postnatal habituation rate was significantly higher in those newborns
who had not participated in the fetal habituation
study than in those who had (7.09/5.4 stimuli versus
4.19/4.1 stimuli) (p/0.01) (Figure 1).
There was a significant positive correlation between the last prenatal habituation rate and the
postnatal one (r/0.42, p/0.01).
Habituation, the ability of an organism to cease
responding to a repeated stimulus, has been proposed as a simple form of non-associative learning.
Unfortunately habituation studies have used very
different methodology and there is a wide range of
definitions of habituation (Table III). We have used
an artificial larynx to generate a vibroacoustic
stimulus which is able to provoke a reflex motor
response in the fetus that is also associated to a
transient acceleration in the FHR. This effect has
been the rationalization of its use in clinical obstetric
practice (13 16).
We chose 24 as the number of stimuli to perform
this study to be able to compare our results with
those from previous reports, the majority of them
using between 20 and 24 stimuli (range 8 50)
(Table III). In comparison, we found a high percentage of fetuses that habituated although the number
of stimuli needed to habituate (habituation rate) was
slightly lower than those previously reported (Table
IV). These differences may be explained by the
special characteristics of the sound we used for
stimulation in terms of quality (novel sound for the
fetuses), frequency, intensity, and a longer interval
between stimuli in order to perfectly identify the
response that caused the stimuli.
We found that the more the number of habituation
procedures the fetuses underwent, the lower the
habituation rates. This decrease in habituation rates
has been previously reported by Van Heteren et al. (3),
who demonstrated that the responses to a repeated
vibroacoustic stimulation could reappear as soon as
10 min after starting the procedure, which suggests
this fact is a result of fetal habituation rather than fetal
exhaustion. However, few studies of human fetal or
newborn habituation have included dishabituation
procedures (i.e. assessment of the reemergence of a
habituated response) to determine if response decrements are the result of reevaluation of information (a
brain process) or fatigue of peripheral receptors.
Sandman et al. (18) have found that the 32-week
human fetus is capable of detecting, habituating, and
dishabituating to an external vibroacoustic stimulus
and this supports the premise that areas of the human
fetal central nervous system critical for detecting and
discriminating information and for learning and
memory have developed by the early third trimester.
Table I. Fetal habituation in each one of the performed tests
Habituation No habituation
N n % n %
Test 1 41 39 95.10 2 4.80
Test 2 32 30 93.75 2* 6.25
Test 3 18 18 100.00
*These two fetuses were the same ones that did not habituate
during the first test.
Table II. Habituation rates according to the number of habituation tests
32 7.89/4.9 6.49/5.1*
18 7.49/4.7 6.09/5.1 5.39/4.0**
SD, standard deviation. *p/0.02, **p/0.1.
1162 N.L. Gonzalez-Gonzalez et al.
Fetal learning and memory have been studied
using habituation testing but only a few studies have
focussed on the persistence of fetal memory into
neonatal life. Most of them did not use a reliable
methodology and their results were difficult to
De Casper and Spencer (9) found significant
differences in the neonatal sucking responses between a group of newborns whose mothers had read
out loud selected passages twice daily for 6 weeks of
pregnancy and a group of controls. Another study
showed that neonatal sucking responses varied when
newborns were exposed to recordings of either
maternal voice or other female voices (10). Along
the same lines, other studies have reported neonatal
ability to recognize maternal voice (19,20), musical
sounds (21 25), or TV tunes (26,27). Several of
these studies suggest the existence of fetal learning
and memory as well as the persistence of learning
into neonatal life. However, they illustrate that this
area of research is very difficult, with many of the
studies having methodological limitations.
James et al. (5) performed a prospective randomized study using music played on the maternal
abdomen in 10 pregnant women who were compared with another group of 10 women who did not
undergo the test. They studied FHR and neonatal
behavioral states. In spite of the small sample size
they found that prenatally exposed neonates showed
more state transitions and spent more time in
awakened states. The authors concluded that prenatal music exposure alters neonatal behavioral
states, suggesting a simple form of fetal learning.
In the present study we designed a simple experimental model by using a real ‘‘novel’’ stimulus for
both fetuses and newborns, as they had never been in
contact with a similar sound. We used a solid liquid
interface in the newborns for simulating as closely as
possible the intrauterine conditions through which
the sound reached the fetuses. Thus habituation
rates were evaluated by using the same procedure in
both fetuses and neonates. The habituation rate of
those newborns who had been stimulated in utero was
significantly lower than that of controls. In other
words, they habituated earlier, suggesting some kind
of persistence of fetal learning and memory into
neonatal life. The neonatal habituation rate of
controls (7.09/5.4 stimuli) was virtually the same as
the fetal habituation rate (7.09/4.6 stimuli), suggesting an excellent fetal neonatal reproducibility of the
test in individuals first-time exposed to that stimulus.
In addition, the existence of a positive correlation
between the prenatal and postnatal habituation rates
suggests that this ability to learn and memorize is not
the same in all the babies and the more stimuli
needed in the fetal period to habituate, the more
stimuli needed in the postnatal period for this.
New born group
Figure 1. Habituation rate to vibroacoustic stimulation in the
Table III. Criteria for defining fetal habituation
Fetal response Number of stimuli
Reference Stimulus Motor/FHR Maximum Frequency Criterium Thabituation
Leader, 1982 (2) Electric brush Motor 50 No response to 5 consecutive stimuli
Van Heteren, 2000 (3) Vibrator 74 dB,
20 9,000 Hz
Motor 24 1/30 s No response to 4 consecutive stimuli
Madison LS,1986 (6) Vibrator Motor 40 10 s Less than 5% movements to 5
Johansson 1992 (7) Vibrator 110 dB
and 3,000 Hz
Motor and FHR 20 1/min Change in FHR B/15 s poststimulus.
Absence of fetal movements
Doherty, 2000 (8) Artificial larynx Motor 40 2/5 s No response to 5 consecutive stimuli
Groome, 1994 (11) Artificial larynx Motor and FHR 8 10 s Decreased fetal movements. No FHR
Shalev, 1986 (12) Door bell Motor and FHR 50 2/10 s No response to 5 consecutive stimuli
Present study Artificial larynx Motor 24 1 min No response to 4 consecutive stimuli
FHR, fetal heart rate.
Persistence of fetal memory into neonatal life 1163
Safety of habituation studies for both fetuses and
newborns may be questioned. Three previous studies
have evaluated hearing function in infants who were
exposed to intrauterine stimulation with artificial
larynxes and no effect could be demonstrated (28
30). To our knowledge, there are no other studies
specifically designed to evaluate side effects of habituation tests. In addition, we have followed the
methodology proposed by Van Heteren et al. (3,17),
who did not report any adverse effect of habituation
tests. Our interval between stimuli was longer (1 min)
than that used in their study (30 s), to give the fetus
enough time to recover, so we could more clearly
evaluate the response to the following stimulus.
In conclusion, our results suggest that those newborns who were stimulated in utero recognized the
stimulus and habituated earlier than those who had
not previously experienced the stimulation. This
suggests that those babies who were stimulated
during fetal life were able to learn and memorize
and both capabilities persisted into their neonatal life.
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Table IV. Fetal habituation to repeated vibroacoustic stimulation
(n) (%) Rate
Leader, 1982 (2) 40 85 10 50
Madison, 1986 (6) 42 96 18 22
Johansson, 1992 (7) 34 64 /3 and B/21
Doherty, 2000 (8) 34 12
Shalev, 1986 (12) 95 20 30
Van Heteren, 2001 (17) 37 81 9.5
Present study 41 95 6.97
1164 N.L. Gonzalez-Gonzalez et al.
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