Although there is data on the spontaneous
behavioural repertoire of the fetus, studies on
their behavioural responses to external
stimulation are scarce.
The aim of the current study was to measure
fetal behavioural responses in reaction to
maternal voice; to maternal touch of the abdomen
compared to a control condition, utilizing 3D
real-time (4D) sonography. Behavioural responses
of 23 fetuses (21st to 33rd week of gestation; N
= 10 in the 2nd and N = 13 in the 3rd trimester)
were frame-by-frame coded and analyzed in the
three conditions.
Results showed that fetuses displayed more
arm, head, and mouth movements when the mother
touched her abdomen and decreased their arm and
head movements to maternal voice. Fetuses in the
3rd trimester showed increased regulatory
(yawning), resting (arms crossed) and self-touch
(hands touching the body) responses to the
stimuli when compared to fetuses in the 2nd
trimester.
In summary, the results from this study
suggest that fetuses selectively respond to
external stimulation earlier than previously
reported, fetuses actively regulated their
behaviours as a response to the external
stimulation, and that fetal maturation affected
the emergence of these differential responses to
the environment.
Introduction
The mother was once regarded as a vehicle, a
conduit for nutrition and waste removal for the
fetus that lived isolated from the outside world
[1&endash;4]. Recent research using
ultrasound techniques however, started to
accumulate evidence on the impact of the
external world on the fetus
[2&endash;8].
Newborns preferentially respond to maternal
voice hours after birth [9&endash;13],
suggesting that the fetus is able to detect
stimuli in utero and form memories of them. The
earliest fetal responses to sound were reported
at 16 weeks of gestation [14], much
before the development of the fetal ear is
complete.
Previous studies on fetal responses to
maternal voice measured changes in fetal heart
rate (FHR) and lead to inconclusive results.
Kisilevsky et al. [15&endash;16] found
an increase, whereas [17] and
[18] reported a decrease in FHR in
response to maternal voice. An increase in FHR
might indicate an arousal response, whereas a
decrease may suggest a possible orientating
mechanism to maternal voice [11].
Hepper, Scott, & Shahidullah [19]
however, found that the voice of the mother
affected FHR the same way as did the voice of a
female stranger with no differential FHR.
A possible reason for the varying outcomes
of these studies might be due to methodological
differences. It is likely that presenting the
maternal voice indirectly such as recorded voice
and via headphones, rather than through bone and
fluid conduction within the body as it happens
with natural speech, may result in an altered
sound experience for the fetus. Indeed, when
Hepper et al. [19] administered maternal
voice both 'in situ' and pre-recorded, they
found that fetuses at 36 weeks of gestational
age (GA) increased FHR responses to the
recording but not to natural maternal
voice.
Proprioception, sensitivity to touch,
develops from 8 weeks GA and by 32 weeks GA most
of the body is sensitive to the light stroke of
a feather [20]. Previous research
reported increases in FHR to vibration from 26
weeks GA with stable and consistent FHR increase
by 32 weeks GA [21]. It was also
reported that in early pregnancy fetuses tend to
move away from stimuli that touch their bodies,
whereas later on they tend to move towards them
[22].
In summary, previous studies show a)
inconclusive results on FHR to maternal voice
and b) that although the fetus is sensitive to
proprioceptive stimulation and maternal touch on
the abdomen is a very commonly occurring natural
stimulus for the fetus, there is currently no
research which has investigated the effect of
maternal touch of the abdomen on fetal
responses. Additionally, although there are
reports on the spontaneous behavioural
repertoire of the fetus, such as fine and gross
motor movements, facial expressions, self-touch
and yawning [23&endash;25], studies on
behavioural responses to external stimulation
are scarce.
The aim of the current study was to measure
fetal behavioural responses in reaction to
maternal voice in situ and tomaternal touch of
the abdomen as well as in control, no sound, no
touch, utilizing 3D real-time (4D) sonography.
Based on previous research
[18&endash;19], it is hypothesised that
fetuses will exhibit a similar attentional
orientation-response to that of the newborn
[26]. Although no prior research on
fetal behavioural responses to maternal touch
exists, it is expected that fetuses, in
particular older fetuses [22] will
respond to touch with a selective increase in
movement, when compared to a control condition
with no stimulation or to maternal voice.
Discussion
While previous research has mainly focused
on FHR responses in reaction to maternal voice
the current study measured fetal behavioural
responses to three conditions: to maternal touch
of the abdomen, to maternal voice compared to a
control condition.
Overall results suggest that maternal touch
of the abdomen was a powerful stimulus,
producing a range of fetal behavioural
responses. Fetuses displayed more arm, head, and
mouth movements when the mother touched her
abdomen as compared to maternal voice in situ.
The increase in their activity was also
indicated indirectly by the decrease of arm
crossing movements in older fetuses. The
difference in the responses by older and younger
fetuses to maternal touch may lend support to
the early observation of [22] that older
fetuses respond preferentially to touch compared
to younger fetuses.
As younger fetuses were in the second
trimester, the results of this study also
indicate that fetuses respond to touch much
earlier than previously described [21]:
in the 21st-25th week rather in the 26th week of
gestation.
Just like armand hand movements of neonates
are far from being random [29, 30],
previous research [30] suggests that
fetal hand and arm movements might also be
directed and intentional [31, 32,33].
Although it is speculative to suggest, it might
well be that the increases in armmovements in
response to maternal touch are also directed
responses towards the source of the stimulation
[34].
The decrease in arm and head movements as a
response to maternal voice supports the results
of [14] using direct maternal voice to
stimulate the fetus. The authors reported a
decrease in FHR to maternal voice in situ as
well as an increase in FHR to recorded voice.
Although the current study did not use recorded
voice, the behavioural quieting to maternal in
situ voice corresponds to the physiological
response of decreased FHR measured by
[14] as well as to the orienting
physiological response [26, 17].
Our study also reported an interesting
behavioural change with maturation, from the 2nd
to the 3rd trimester. Regardless of the
experimental condition, fetuses in the 3rd
trimester displayed more self-touch (hands
touching the body) when compared to fetuses in
2nd trimester. This observed increase in
self-touch might be due to the increased tactile
sensitivity of the skin as fetuses develop. As a
consequence fetuses may seek out proprioceptive
stimulation just as neonates were reported to do
[35].
Fetuses in the 3rd trimester also spend more
time with crossed arms compared to fetuses in
the 2nd trimester. This behaviour most likely
indicates that the fetus is resting, and if so,
this finding is in support of previous findings
[23], which reported an overall decrease
of movements as fetuses mature. However as the
fetus grows rapidly during the third trimester,
the uterine environment becomes increasingly
smaller limiting fetal motor behaviour.
Therefore less movement and more touching the
body was to be expected. It is also space saving
to fold the arms in front of the body during
rest. However, fetuses in 3rd trimester cross
their arms more often in response to maternal
voice as compared to the touch condition. This
behaviour is one of the behaviour activity
responses to maternal touch, thus a decrease in
arm-crossing behaviour might be a consequence of
the increase of other, arm, head, mouth
movements and indicates an increased activity of
the fetus.
Older, third trimester fetuses yawned more
during maternal voice stimulation compared to
the control condition and also showed a tendency
to yawn more during maternal touch. Fetuses in
the 2nd trimester, however, showed no
differential change in their yawning. The
observed increase of yawning in older fetuses
stands in contrast to reports [24], who
found a decrease rather than an increase in
yawning frequencies from 28 weeks of pregnancy.
Although the mechanisms and functions of fetal
yawning are still unexplored most recent
theories suggest its connection to activity
dependent brain maturation of regulatory
behaviours [25]. Overall increased
regulatory (yawning), resting (arms crossed) and
self-touch responses to external stimuli were
observed among older fetuses. Such results could
reflect the maturation process of the nervous
system as the fetus develops.
In summary, the results from this study
suggest that fetuses selectively respond to
external stimulation earlier than previously
reported, fetuses actively regulate their
behaviours as a response to the external
stimulation, and that fetal maturation affects
the emergence of such differential responses to
the environment.
Mothers, fathers and other family members
talk and even sing to the fetus throughout
pregnancy with communicative intent. Many report
changes in the fetal behaviour as a response to
such communication. And although we used the
term 'touch', the condition however was not
direct skin-to-skin contact but an indirect
stimulation of the fetus via stroking the
abdomen applying slight pressure. Similarly to
talking to the fetus, most mothers and even
fathers attempt to communicate with and regulate
the behaviour of the fetus via stroking of the
mother's abdomen as a response to the kicking or
positional movements of the fetus. Even the
expecting mothers' mood is affected by massaging
the abdomen resulting in reduced depression
[36].
As earlier research by Zoia et al [31,
33] showed, the kinematic patterns of the
movements of fetuses reflect intentional
actions, and advanced motor planning, therefore
it is plausible to suggest that the observed
fetal responses to the voice and touch in the
present study may have a communicative
intent.
