Fetal homologue of infant crying

Abstract

Four behavioural states are recognised in the human fetus and are comparable to those of the neonate: 1F (quiet sleep), 2F (active state), 3F (quiet awake), and 4F (active awake). State 5, or crying, is not considered to have a fetal correlate. In a study assessing the effects of exposure to tobacco and cocaine during pregnancy on fetal response and habituation to vibroacoustic stimulation, what appears to be the fetal homologue of crying was observed. These behaviours were seen on ultrasound, and have been captured on video recordings and include: an initial exhalation movement associated with mouth opening and tongue depression, followed by a series of three augmented breaths, the last breath ending in an inspiratory pause followed by an expiration and settling. This is the first report/video documenting these behaviours and suggests the possibility of a state 5F.

Full text

ORIGINAL ARTICLE
Fetal homologue of infant crying
J L Gingras, E A Mitchell, K E Grattan
...............................................................................................................................
A video clip can be
downloaded from the
Archives of Disease in
Childhood website (http://
adc.bmjjournals.com/
supplemental/).
See end of article for
authors’ affiliations
.......................
Correspondence to:
Professor Mitchell,
Department of Paediatrics,
University of Auckland,
Private Bag 92019,
Auckland, New Zealand;
e.mitchell@auckland.ac.nz
Accepted 5 February 2005
Published Online First
27 April 2005
.......................
Arch Dis Child Fetal Neonatal Ed 2005;90:F415–F418. doi: 10.1136/adc.2004.062257
Four behavioural states are recognised in the human fetus and are comparable to those of the neonate: 1F
(quiet sleep), 2F (active state), 3F (quiet awake), and 4F (active awake). State 5, or crying, is not
considered to have a fetal correlate. In a study assessing the effects of exposure to tobacco and cocaine
during pregnancy on fetal response and habituation to vibroacoustic stimulation, what appears to be the
fetal homologue of crying was observed. These behaviours were seen on ultrasound, and have been
captured on video recordings and include: an initial exhalation movement associated with mouth opening
and tongue depression, followed by a series of three augmented breaths, the last breath ending in an
inspiratory pause followed by an expiration and settling. This is the first report/video documenting these
behaviours and suggests the possibility of a state 5F.
F
ive distinct behavioural states are recognised in the
neonate: 1, quiet sleep; 2, active sleep; 3, quiet awake; 4,
active awake; 5, crying. In the fetus, four distinct
behavioural states 1F, 2F, 3F, and 4F have been identified
and correspond to the neonatal behavioural states 1–4
(table 1).
12
State 5, or the crying state, has no reported fetal
correlate. We describe what we believe is the first documen-
tation of crying behaviours in the fetus. These behaviours
were elicited during vibroacoustic stimulation (VAS), which
was performed as a research study assessing the effect of
exposure to tobacco and cocaine during pregnancy on fetal
response and habituation to VAS.
3
METHOD
Fetal ultrasound assessments were performed on up to three
occasions (29–31, 32–35, and 36+ weeks gestation). These
assessments were made in a semidarkened room using B
mode ultrasonography (Corometrics Aloka 650 ultrasono-
graph). The ultrasound transducer was positioned for a
lateral-oblique view of the fetus. Fetal eye movements and
gross body movements were observed in real time by an
observer and were recorded on video. Fetal heart rate was
measured by continuous wave Doppler (Corometrics Fetal
Monitor 145) and recorded continuously on the built in, dual
channel, strip chart recorder. Behavioural state was assessed
from these sources.
The fetus was observed unperturbed for 20 minutes. After
this initial observation period, and when it appeared to be in
a stable state (quiet or active sleep), the fetus was challenged
with VAS. The VAS was provided by an artificial larynx
(model 5c; Western Electric) that emits fundamental tones of
about 100 Hz and 95 dB and was mechanically altered to
provide exactly 0.5 second of stimulation. This duration was
selected because longer stimulus durations have been
associated with excessive fetal movements and prolonged
tachycardia.
4
The physiological intrauterine noise intensity
has been reported to be about 85 dB.
5
No adverse effects have
been reported at this intensity, duration, and frequency.
4
After stimulation, the fetus was observed for a blink-startle
response for a duration of 10 seconds.
6
The study had ethical approval from the Charlotte Medical
Center institutional review board, and the parents gave
written informed consent for the study.
Case report
The mother was an African-American primigravida, who
smoked ,10 cigarettes a day. She did not abuse cocaine. The
female fetus was assessed at 33 weeks gestation when the
‘‘cry’’ behaviours were seen. There were no complications
during the pregnancy. At 40 weeks gestation there was
spontaneous onset of labour. There was a normal vaginal
delivery, and the infant’s birth weight was 3555 g.
The video clip (which can be found at http://adc.
bmjjournals.com/supplemental/) and figs 1–3 show what
we believe is the fetal homologue of crying. The video begins
with the quiet fetus before presentation of the VAS. The fetus
is initially seen in an oblique view. The stimulus is presented.
The fetus startles and turns her head to a lateral view, and is
seen in profile (fig 1). The fetus then initiates behaviours
consistent with crying. There is a brief expiration that is
followed by a deep inspiratory phase with a subsequent
pronounced expiratory phase. This expiration is associated
with jaw opening, taut tongue, and chest depression (fig 2).
It is immediately followed by three augmented breaths with
progressive increase in chest rise and head tilt (fig 3). Each
end inspiration is marked by chin quiver. The last augmented
breath ends in an inspiratory pause, followed by an
expiration and settling. Settling is associated with a turn of
F415
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the fetal head to the oblique position, mouthing, and
swallowing. This pattern of behaviour was seen again when
a repeat VAS was presented to the fetus at about one minute
after the initial cry. These behaviours are shown in the video
and presented in a conceptualised form in fig 4.
This behavioural response was not an isolated case. Once
recognised, more episodes of these behaviours were seen
during the VAS testing of other fetuses. Ten subjects showed
fetal crying behaviour, three of whom showed all of the
characteristics on two separate occasions. Fetal crying
behaviour was seen three times at the first assessment
(gestational age 28–31.9 weeks), four times at the second
assessment (32–35.9 weeks), and on six occasions at the
third assessment (.36 weeks). Four mothers smoked cigar-
ettes during pregnancy, three smoked and used cocaine, and
three neither smoked nor used cocaine. The study population
consisted of three groups of mother-fetal dyads: (1) cigarette
smokers (n = 54), (2) cocaine users (n = 30), and (3)
controls (n = 60). Only one infant had a low Apgar score at
one minute and none at five minutes. Six of the infants were
female, and four were male. Birth weight and gestation did
not differ from the sample as a whole (range 2637–4138 g
and 36.7–41.7 weeks).
DISCUSSION
Crying is a complex, rhythmical series of sounds that requires
precise coordination between various motor systems includ-
ing the musculature of the face, airway, and respiration.
7
Fundamental to postnatal cry is vocalisation. Thus newborn
and infant crying consists of both a vocal and non-vocal
component. Hopkins
8
suggests that the non-vocal accompa-
niments of crying are developed before birth, the vocal
component being established with transition to the extra-
uterine life. The observations recorded from fetal ultrasounds
support the concept that the fetus is capable of the complex
motor behaviours that accompany the crying state.
These observations may have further developmental
implications, as the expression of crying implies more than
execution of a motor pattern. Crying requires reception of a
stimulus, association of that stimulus with a negative
Table 1 Neonatal and fetal states
Neonatal
behavioural
state Descriptors Neonatal behaviours
Fetal state
correlate Fetal behaviours Fetal heart rate pattern
1 Quiet, asleep Regular respirations,
non-REM sleep
1F FB: regular, if present A: Variability (10 beats/min), isolated
accelerations associated with
movement
FBM: rare gross movements,
non-discriminatory
FEM: absent
2 Active, asleep Irregular respirations,
REM sleep, activity
non-discriminatory
2F FB: irregular, if present B: Variability (10–20 beats/min),
frequent accelerations of 10–
20 beats/min
FBM: small body movements,
gross, non-discriminatory, episodic
FEM: absent
3 Quiet, awake Regular respirations,
no gross activity
3F FB: regular, if present C: No accelerations, rate oscillates
more regularly than in BFBM: no gross movements
FEM: present
4 Active, awake Irregular respirations,
physically active
4F FB: irregular, if present D: ‘‘Unstable’’ rate, variability up to
25 beats/min, accelerations of 25–
30 beats/min, occasional sustained
tachycardia
FBM: gross and small movements,
continual
FEM: present
5 Crying Irregular respirations,
physically active
Described here
FB, Fetal breathing; FBM, fetal body movement; FEM, fetal eye movement.
Figure 1 The fetus is seen in profile. The upper position of the anterior
chest wall is marked with a horizontal line at baseline. The initial angle of
the chin is also shown.
Figure 2 The beginning of the ‘‘cry’’ is shown. The head is seen in
profile, the mouth is open, the anterior chest is below the original
position, indicating the initial expiratory movement.
F416 Gingras, Mitchell, Grattan
www.archdischild.com

connotation, and incorporation of an appropriate motor
response that itself recruits a complex pattern of more
primitive motor sequences. The sensory aspect of the cry
response—that is, reception of the sound—implies intact
afferent processes. Recognition of the stimulus as negative
indicates development of more rostral brain sites that
mediate affect and further integrate that affect with a motor
response. The expression of crying thus indicates a several
stage maturation of sensory reception, processing of signals
as potentially deleterious, a dimension of affect, and
recruitment of an appropriate response. Of this sequence,
demonstration of affective integration, which incorporates
limbic structures, implies more rostral neural maturation.
The ability of the fetus to show affective integration of motor
responses is supported by the observation that the fetal
crying behaviours were seen only after VAS.
Crying consists of a sequence of vocal and non-vocal
behaviours. Although crying is phenomenologically self
evident in both the term and preterm infant, there is
no unified or accepted definition that incorporates all
aspects of the cry behaviour. Well described are the facial
accompaniments of cry: grimace or frown, trembling of the
chin, swallowing, and eye closure.
8
Others describe move-
ment of the extremities.
79
These behaviours are tightly linked
to the respiratory cycle.
10
In the newborn, each cry cycle
displays a consistent displacement of respiratory volume,
suggesting a precise coordination between various motor
systems and that of the respiratory system.
11
Cries are
produced primarily in the expiratory phase; however, the
newborn is capable of inspiratory ‘‘voicing’’.
12
Thus Wolff’s
13
classic description of infant cry as a rhythmic repetition
consisting of an expiratory sound lasting 0.6–1.3 seconds, a
brief pause of 0.2 second, and an inspiratory sound or whistle
of about 0.1–0.2 second followed by another pause of
0.2 second before the next sound made on expiration,
continues to provide the most comprehensive description of
the infant cry. The behaviours shown in the video correspond
to the neonatal cry with the vocalisation component
occurring during the expiratory phases.
By 20 weeks gestation, the fetus possesses the complete
motor repertoire necessary for cry behaviours: coordinated
breathing efforts, jaw opening, mouthing, chin quiver,
tongue extension, and swallowing.
14–16
Furthermore, it is
well known that the preterm infant of about 24 weeks
gestational age is capable of producing crying sounds
17 18
and
can respond to environmental noise.
19
Thus the fetus is
capable of responding to sound and other perturbations with
highly coordinated movements that mimic the temporal and
behavioural components of the extrauterine cry. This
phenomenon suggests a prenatal origin of crying, and sup-
ports the contention that the fetus does have a comparable
state 5—that is, state 5F. This concept provides a develop-
mental continuity between the prenatal and postnatal life.
The method of Nijhuis et al
2
for determining fetal state
required that the three state variables (body movements, eye
movements, and heart rate pattern) are maintained for three
minutes. This process follows the strategy used for the
assessment of state in the newborn.
20
Periods of less than
three minutes are referred to as periods of coincidence, and
may represent chance occurrence. It may be inappropriate to
apply the three minute criterion to 5F, as crying in the
neonate is often of shorter duration. In our case, the observed
cry behaviours lasted 15–20 seconds.
The fetal ‘‘cry’’ behaviour, or state 5F, was seen in our
study only after VAS. This observation may suggest that the
‘‘fetal cry’’ is elicited only when the fetus is disturbed. The
20
Time (seconds)
Prolonged expiration
with jaw opening
3 augmented breaths
Settling
Transducer
movement
Short
expiration
Initial inspiration
Baseline
Chest movement
InspirationExpiration
0 5 10 15
Figure 4 Graphic representation of the movement of the anterior chest wall during one cry cycle. The notations identify the associated behaviours. The
asterisk shows when the chin quiver occurred.
Figure 3 The notations mark the increase in chest elevation and head
tilt during the three augmented breaths.
Fetal crying F417
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behaviours were seen in all gestational ages studied,
indicating that the behaviour occurs as early as 28 weeks
gestation, and possibly earlier. The behaviour was observed
equally in controls (non-smokers and no cocaine use),
suggesting that these behaviours are not specific to tobacco
or cocaine exposure.
Finally, what we have observed is similar to the rare, but
well authenticated, phenomenon of vagitus uterinus, a term
used to describe the audible cry of the fetus in utero.
21
Cases
of vagitus uterinus are generally found at term, are associated
with ruptured membranes that have allowed air to enter the
uterus, and some operative intervention usually has occurred
which has stimulated the fetus. Our case occurred seven
weeks before delivery, and, although the body and facial
movements were consistent with crying, an audible cry was
not heard.
ACKNOWLEDGEMENTS
We thank the Education Media Centre, University of Auckland for
the production of the video clip and figs 1–3, and Professor Ron
Harper for helpful comments on the manuscript. EAM is supported
by the Child Health Research Foundation, Auckland, New Zealand.
Authors’ affiliations
.....................
J L Gingras, K E Grattan, The SIDS CARE Center, Carolinas Medical
Center, Charlotte, NC, USA
J L Gingras, University of North Carolina-Chapel Hill, Chapel Hill, NC,
USA
E A Mitchell, Department of Paediatrics, University of Auckland,
Auckland, New Zealand
The project was funded by NICHD (National Institutes of Child Health
and Development) and NIDA (National Institute on Drug Addiction)
(RO1: DA05949).
Competing interests: none declared
To access the video clip mentioned in this paper please ensure that you
have QuickTime installed on your computer.
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What is already known on this topic
Four behavioural states are recognised in the human fetus
and are comparable to those of the neonate: 1F (quiet sleep),
2F (active state), 3F (quiet awake), and 4F (active awake).
State 5, or crying, is not considered to have a fetal correlate.
What this study adds
In a study assessing the effects of exposure to tobacco and
cocaine during pregnancy on fetal response to vibroacoustic
stimulation, we observed what appears to be the fetal
homologue of crying. This is the first report/video document-
ing these behaviours and suggests the possibility of a fetal
state 5F.
F418 Gingras, Mitchell, Grattan
www.archdischild.com