Prenatal Stress Exposure Alters

Postnatal Behavioral Expression -

Under Conditions of
Novelty Challenge in
Rhesus Monkey Infants
MARY L. SCHNEIDER
Department of Therapeutic Science
Vniuersity of Wisconsin
Madison, Wisconsin

This prospective study investigated whether mild maternal stress during pregnancy could alter
the behavioral and affective responses in rhesus monkey infants in a complex, novel environment.
Twenty-four rhesus monkey infants were tested on three occasions at 6 months of age in a novel
environment. Twelve infants were derived from mothers exposed to a daily 10-min mild stressor from
Day 90 to Day 145 postconception, while 12 were derived from mothers undisturbed during pregnancy.
Prenatally stressed infants demonstrated more disturbance behavior, and lower levels of gross motor/
exploratory behavior. Moreover, half of the prenatally stressed infants showed an abnormal response,
falling asleep, while none of the control infants displayed this behavior. Males exhibited more clinging
to surrogates, while females spent more time in gross motorlexploratory behaviors, with prenatally
stressed males tending to spend the least time in gross motor/exploratory activity. 0 1992 John Wiley
& Sons, Inc.

A growing body of literature has documented that the development of human

behavior can be influenced not only by inherited characteristics and postnatal
events but also by the intrauterine environment via prenatal exposure to alcohol,
drugs, nutrition, and maternal emotional distress. However, the effects of maternal
emotional distress during pregnancy on the developing fetus and its subsequent
behavioral characteristics has received only limited attention. Whereas some stud-
ies in infants and children have suggested that stressful life events during pregnancy
are associated with lower birth weights (Field, Sandberg, Quetel, Garcia, & Rosa-
rio, 1985; Sontag, 1941), increased infant irritability (Ottinger & Simmons, 1964),

Reprint requests should be sent to Dr. Mary L. Schneider, Department of Therapeutic Science, 2175
Medical Science Center, 1300 University Avenue, Madison, WI 53706-1532, U.S.A.

Received for publication 22 October 1991

Revised for publication 9 July 1992
Accepted at Wiley 13 July 1992

Developmental Psychobiology 25(7):529-540 (I 992)

0 1992 by John Wiley & Sons, Inc. CCC 0012-1630/92/070529-12
530 SCHNEIDER

obstetrical complications (Field et al., 1985; Grimm, 1961) and subsequent develop-
mental problems including lowered IQ, hyperactivity, and speech and language
problems (Lederman, Lederman, Work, & McCann, 1978; Meijer, 1985), others
have failed t o confirm these results (Chalmers, 1983). Many inconsistencies in the
human studies are due to methodological problems, including: I ) failure to control
for postnatal effects on the infant; 2) inadequate control of variables that may
covary with prenatal stress, such as obstetric medication, smoking, alcohol, or
other drug use; and 3) reliance on retrospective data (Copans, 1974).
More consistent findings have emerged from animal models. There is evidence
that stress t o rats during pregnancy produces numerous deleterious effects to the
fetus. Several types of stress have been employed, and one of the most well-
established effects is the inadequate masculinization of sexual patterns in prena-
tally stressed male rats (Ward, 1972, 1977; Dorner, Gotz, & Docke, 1983; Rhees
& Fleming, 1981). These alterations in sexual behaviors are believed to result from
an abnormal pattern of testosterone during fetal life in such offspring (Ward &
Weisz, 1980).
In addition, there are also several reports that indicate that prenatal stress in
rats may be associated with an increased mortality rate in newborns (Politch &
Herrenkohl, 1979; Pollard, 1984; Rojo, Marin, & Menendez-Patterson, 1985),
lowered birth weights, and retardation of fetal growth (Pollard, 1984). In addition,
prenatally stressed rodents were impaired in early motor coordination and exhib-
ited less activity in an open-field test (Grimm & Frieder, 1987). Other researchers
have found a decrease in locomotion in the open-field test in prenatally stressed
rodent offspring (Thompson, 1957; Fride & Weinstock, 1988), indicating an in-
creased vulnerability to stressful events (Fride, Dan, Feldon, Halevy, & Wein-
stock, 1986).
Despite the relatively large number of rodent studies, the issue of prenatal
stress has received limited attention in nonhuman primate studies. However,
nonhuman primates are more similar to humans than are rodents during the infancy
period (Harlow & Harlow, 1966; Schneider & Suomi, 1992) and therefore the
nonhuman primate model is a preferable model for investigating the effects of
prenatal stress on offspring emotionality. The nonhuman primate studies that exist
have linked maternal disturbance during pregnancy to transient asphyxia in the
rhesus monkey fetus (Myers, 1975). Exposure of pregnant pigtailed macaques to
stressful situations resulted in an increase in miscarriage rates in those females at
low risk for a poor pregnancy outcome (based on prior pregnancy outcomes)
(Sackett, 1981). In offspring of stressed pigtail macaques, higher dermatoglyphic
asymmetry was noted (high asymmetry was associated with increased perinatal
mortality) (Newell-Morris, Fahrenbruch, & Sackett, 1989). Because exposure t o
stress is associated with a rise in glucocorticoids (Coe et al., 1978), female rhesus
monkeys who were administered glucocorticoids during midgestation were exam-
ined, and degenerative changes in fetal hippocampal neurons were noted (Uno et
al., 1990). Finally, we have recently shown that daily exposure of pregnant rhesus
monkeys t o a 10-min stressor (removal from home cage and confinement in small
cage and coupled with three unpredictable noise bursts) during mid-late gestation
resulted in offspring with lower birth weights, impaired motor abilities, and in-
creased distractibility (Schneider, in press); delays were also noted on subsequent
learning tasks (Schneider, 1992) when compared to offspring from undisturbed
 PRENATAL STRESS AND NOVELTY CHALLENGE IN RHESUS 531

females. In addition, when pregnant rhesus monkeys were exposed to a 2-week

period of adrenocorticotropic hormone, the postnatal early neuromotor develop-
ment of offspring was affected in a manner similar to that observed after psycholog-
ical stressors (Schneider, Coe, & Lubach, 1992). Finally, squirrel monkey infants
derived from pregnancies wherein swial relationships were repeatedly disrupted
exhibited poorer motor abilities and shorter attention spans compared to controls
(Schneider & Coe, in press).
In the present study, we investigated further the suggestions that mid-late
gestational stress compromises the developmental outcome of the offspring, partic-
ularly with regard to vulnerability to stressful situations. Therefore, the behavioral
reactions of prenatal stressed and control infants when exposed to a complex,
novel environment were assessed. Reaction to a novel environment was selected
as a stimulus because results from prior nonhuman primate studies have shown it
to be a sensitive index of the ability to cope with a stressful situation (Ferguson &
Bowman, 1990; Laughlin & Bowman, 1984; Mason & Green, 1962; Mineka, Gun-
nar, & Champoux, 1986; Schneider, Kraemer, & Suomi, 1991). Because previous
work has linked prenatal stress to impaired coping in the face of novelty (Fride et
al., 1988), it was hypothesized that the prenatally stressed offspring would show
signs of increased behavioral disturbance under stressful conditions in comparison
to the control subjects.

Methods
Subjects
The subjects were 24 infant rhesus monkeys (Macaca muiutta), 12 control (7
male, 5 female) and 12 experimental (6 male, 6 female), that were separated from
their mothers on Day 2 postpartum and reared for the first 30 days postpartum in
the laboratory nursery according to the procedure described by Ruppenthal(l979).
Infants were nursery reared to prevent potential confounds due to differential
maternal treatment. During nursery rearing, subjects were housed individually in
41 x 51 X 42 cm cages enriched with the following: a cloth-covered, water-filled
plastic pillow, a cloth-covered movable surrogate, two loops of plastic garden hose
serving as a climbing apparatus, and a variety of brightly colored manipulatable
infant toys rotated among infants daily (Schneider & Suomi, 1992). They were
socialized daily for 15 min in a play group with another infant from a similar
experimental condition. All subjects had free access to Similac infant formula.
At approximately 30 days of age, the infants were placed in peer groups
consisting of 3 infants each from a similar prenatal stress condition.' Peer groups
were housed in standard wire mesh quad-cages (66 x 88 x 132 cm) that contained
loops of plastic garden hose as a climbing apparatus, a variety of brightly colored
manipulatable infant toys that were rotated daily, and three cloth-covered movable
surrogates. The infants received three 175-ml bottles of Similac each morning and
three 175-ml bottles of Similac each evening until the youngest animal was 6
months old. Purina monkey chow and water were available ad libitum prior to
weaning from Similac. Following weaning, monkey chow was rationed and weight
gain was monitored.
532 SCHNEIDER

Maternal Characteristics
The infants were derived from healthy laboratory-reared female rhesus mon-
keys. Females were randomly assigned to control or stress groups. There were no
differences in age, weight, or parity between groups. All females were multiparous,
and none had a history of recurrent fetal loss due to miscarriage or stillbirth. All
females had prior social experience. At the time of this study they were members
of a breeding colony; they were singly caged with free access to water, fed a
standard diet (Purina monkey chow), and kept under standard light/dark schedule
(16:8) and temperature (21 +- IOC).

Maternal Treatment
The stress stimulus was administered to the experimental females from Day 90
to Day 145 postconception (term is 165 days). Gestation age was assessed as the
interval between the 1st day of the 3-day timed mating period of the mothers and
parturition. The stress treatment was administered five times per week at 1600 hr.
It involved removing the pregnant females from their home cages in a standard
transport cage, transporting them to a darkened room, and administering three
noise bursts randomly during a 10-min period. The noise burst consisted of an
alarm horn that produced a 115-db sound at 1 m, 1300 Hz. The cages were ordered
in the room to provide an equivalent exposure to the sound for all stressed females.
During the remainder of the day both control and stressed females were housed
under identical conditions, undisturbed except for necessary routine husbandry
procedures.

Apparatus
The area that served as the infant testing room (hereafter referred to as the
playroom) was a large room (2.4 x 2.0 x 2.2 m) containing a variety of movable
and nonmovable wire mesh climbing and sitting platforms. Testers observed the
monkeys through a glass observation window (2.3 x 1.3 m). The interior of the
playroom was lighted; the outer observation room was darkened. This increased
the testers’ ability to view the monkeys and decreased the monkey’s view of the
testers.

Procedure
When the subjects were approximately 6 months old, each peer group consist-
ing of 3 subjects was given a 15-min testing session in the playroom each day for
3 consecutive days. None of the subjects had previously been tested in the play-
room. The groups were transported from the home cage to the playroom in a
standard transport cage. The transport cage was placed in front of a small opening
leading into the playroom and the infants were given 5 min to emerge from the
transport cage. Subjects that had not emerged from the transport cage within 5
min were removed by the tester and placed into the playroom. Once all 3 subjects
were in the playroom, the 15-min scoring began.
 PRENATAL STRESS AND NOVELTY CHALLENGE IN RHESUS 533

Data Collection
The 15-min session was divided into three consecutive 5-min scoring periods.
Three observers, each randomly assigned to I of the 3 infants in the group, were
seated in front of the glass window and simultaneously recorded the frequency
and duration of behaviors falling into predefined categories. Observers rotated
subjects across the 5-min periods so that each observer scored each of the three
infants once. All observers were trained to reliability, rs > .90. The frequency and
duration of nine behaviors were recorded on Radio Shack TRS-80 Model 102
Portable Computers. The behaviors and their operational definitions are delineated
as follows: (a) contact cling-contact of own ventral body surface with another
infant; (b) on surrogate-contact with an artificial mother-surrogate; (c) seff-
directed-scratching, grooming, grasping, biting, or sucking any part of own body;
(d) locomotion-any change in physical location of self, excluding locomotion
used in a play bout and climbing; (e) environmental exploration-oral, manual, or
pedal exploration/manipulation of the inanimate environment; (f) visual expfora-
tion-visual exploration of the environment in the absence of other behaviors; (8)
climb-any self-induced change in location of self where the infant was in contact
with ramps or ledges; (h) plays-activity bout involving play face, bobbing, nonag-
gressive biting, chasing, mouthing, pulling at another infant’s body, lunging at
another infant, mount attempts, and receiving a mount from another infant; in-
cludes self-play; and (i) sleep-absence of all social, exploratory, and locomotor
activity, eyes closed. At the end of the test session, the subjects were hand-
captured, placed into the transport cage, and returned to the home cage. This
procedure was repeated for 3 consecutive days.

Data Analysis
The duration data from this study were analyzed in three stages. First, the
scores from eight behavioral categories were collapsed into two categories in order
to yield a single composite score for disturbance behavior and a single composite
score for gross motor/exploratory behavior. This procedure is commonly done in
primate studies (Clarke & Mason, 1988)because individual subjects tend to express
disturbance and/or exploratory behavior in a unique manner. For example, one
subject might express distress by clinging to its surrogate, a second subject might
cling to cagemates, while a third might clasp itself. Therefore, it is useful to
combine behaviors that reflect the same domain in order to capture the underlying
meaning or essence of the behavioral response. The disturbance category included
the foIlowing behaviors: clinging to cagemates, clinging to surrogate, and self-
directed behaviors. The gross motor/exploratory category included locomotion,
environmental exploration, climbing, playing, and visual exploration of the envi-
ronment. The sleep category was not included with either of these categories
because it was considered to reflect an independent domain.
Next, the subjects’ reactions to the novel environment were examined for
possible systematic variance due to the prenatal stress condition, gender, and
repeated testing (across the 3 testing days and across the 3 scoring periods). For
every subject, scores recorded each day during the three 5-min testing periods
were averaged to yield a mean for each day (Day I, Day 2, and Day 3). In addition,
534 SCHNEIDER

z
0
u)
4001
300
T
0-
PRENATALLY STRESSED

u)
y1
u)

E
n
200
z
0
E
cn
z 100
3
z

0
DISTURBANCE EXPLORATORY SLEEP

BEHAVIORAL CATEGORIES

Fig. 1. Mean duration of behavior in a stressful situation as a function of prenatal condition

(stress, control). Bars represent standard errors.

scores recorded during each 5-min period each testing day were averaged across
days to yield a mean for each period (Period 1, Period 2, and Period 3). Each set
of means was then subjected to a three-way analysis of variance, with prenatal
condition and sex as the between-subject variables and days (Day 1 vs. Day 2 vs.
Day 3) or Periods (Period 1 vs. Period 2 vs. Period 3) as the repeated measure.
When there was a large difference in variance across groups, the nonparametric
Mann-Whitney U test was used on the data because it is not as affected by
violations of assumptions about normality and equal variances.

Results
Prenatal Condition
The results of the present experiment indicated that the prenatally stressed
infants exhibited more disturbance behavior than control subjects in a novel envi-
ronment, whereas the control subjects displayed higher levels of gross motor/
exploratory behavior.* Mean levels of disturbance behaviors, gross motor/explor-
atory behaviors, and sleep are shown in Figure 1. Analysis of variance demon-
strated significantly lower durations of gross motodexploratory behaviors for
the prenatally stressed subjects compared to controls, 72 t- 24 and 125 S 12,
respectively, F(1, 22) = 4.76, p < .04. Prenatally stressed offspring exhibited less
climbing, visually explored the environment less, and were consistently lower in
locomotion, environmental exploration, and play (see Table 1).
The prenatally stressed infants displayed significantly higher durations of dis-
turbance behavior compared to controls, 309 2 44 versus 198 k 23, F(1, 22) =
5.20, p < .04 (see Fig. 1). They were consistently higher on contact cling, cling to
surrogate, and self-directed behavior.
 PRENATAL STRESS AND NOVELTY CHALLENGE IN RHESUS 535

Table 1
Means and Standard Errors for Playroom Behaviors
for Prenatally Stressed and Control Infants
Prenatal Stress Control
Behavior Mean ( S E ) Mean (SE)
Locomotion 35(12)
Environmental exploration 24(8)
Climb 10(4)
Play 1.1(.4)
Visual exploration 21)
Contact cling 18 l(28)
Cling to surrogate 53(22)
Self-directed 75(22)
~ ~

Note. a Mann Whitney U test.

Finally, prenatally stressed infants exhibited significantly higher durations of

sleep behavior, Z = -2.44, p < .05, Mann-Whitney U test.

Gender
The means and standard deviations for males versus females are shown in
Table 2. Males demonstrated longer duration of clinging to surrogate whereas
females spent more time in gross motor/exploratory behavior, F(1, 22) = 4.35,
p < .05.

Gender X Prenatal Condition

There were no statistically significant Sex x Prenatal Condition interactions.

Days of Testing
There was a significant main effect for days of testing. Gross motor/exploratory
behavior increased significantly across days of testing, F(2,44) = 12.66, p < .0001,
whereas disturbance behaviors decreased significantly across days of testing,

Table 2
Means and Standard Errors for Playroom Behaviors
for Males and Females
Males Females
Behavior Mean ( S E ) Mean ( S E )
Locomotion
Environmental exploration
Climb
Play
Visual exploration
Contact cling
Cling to surrogate
Self-directed
Sleep
536 SCHNEIDER

K
W
Q.

0
v)
z
100 + STRESSEDMALES
0 -.f- STRESSEDFEMALES
!i
v)
-I)- CONTROLMALES
+ COMROLFEMALES

0
1 2 3

DAYS OF TESTING

Fig. 2. Mean duration of gross motor or exploratory behaviors across testing days as a function
of prenatal condition (stress, control) and sex.

F(2, 44) = 10.44, p < .002. There were no significant interactions for Prenatal
Condition x Days of Testing or for Gender x Days of Testing for either distur-
bance or gross motor/exploratory composite scores. There was a marginally sig-
nificant three-way interaction for Prenatal Condition x Sex x Days of Testing for
gross motor/exploratory behaviors F(2, 40) = 2.80, p < .07 (See Fig. 2).

Testing Period
Analysis of variance yielded a significant main effect for testing period (Period
1 vs. Period 2 vs. Period 3) in that gross motor/exploratory behaviors increased
across time periods, F(2,44) = 17.69, p < .OOOl; disturbance scores failed to show
an effect. There were no significant interactions for Prenatal Condition X Testing
Period, however, there was a significant effect for Sex x Testing Period for
disturbance behaviors. (See Fig. 3). Males showed an increase in disturbance
behavior across testing periods while females displayed a decrease in such behav-
iors, F(2, 44) = 3.79, p < .03. There were no significant three-way interactions
for Prenatal Condition x Sex x Testing Period.

Discussion
The reactions of prenatally stressed and control infants to an unfamiliar envi-
ronment were strikingly different. Prenatally stressed infants tended to show more
disturbance behavior and half of the prenatally stressed infants showed an abnor-
mal response, falling asleep, during this brief time in the playroom while none of
the control infants displayed this behavior. Instead, the control infants exhibited
higher levels of gross motor/exploratory behavior. In addition, males tended to
 PRENATAL STRESS AND NOVELTY CHALLENGE IN RHESUS 537

$
300
a
W
n

---o--.
MALES
FEMALES
1
,
0.0 1 .o 2.0 3.0

SESSIONS

Fig. 3. Mean duration of disturbance behaviors across testing periods in a stressful situation as
a function of sex. Bars represent standard errors.

show lower levels of exploratory behavior; there was a suggestion that this may
be particularly true for prenatally stressed males.
The finding that prenatal stress negatively affected environmental exploration
under conditions of novelty challenge was not surprising, given similar findings in
rats (Grimm & Frieder, 1987; Fride et al., 1986). Furthermore, striking similarities
have been reported among human children subject to stressful events prenatally.
For example, Meijer (1985) examined offspring of mothers undergoing stress during
pregnancy during the Israeli 6-day war and found they were significantly more
tense and anxious than controls.
The underlying mechanism of the prenatal stress effect is not known. However,
studies have shown that maternal hormones influence the developing fetal brain
and provide the basis for future behavioral characteristics (Joffe, 1978). Further,
studies with baboons have demonstrated that administration of catecholamines to
the mother during pregnancy produced fetal asphyxia through uterine vasocon-
striction (Morishima, Pedersen, & Finster, 1978). Others have suggested that
maternal pituitary hormones alter the fetal hippocampus (Uno et al., 1990), result-
ing in long-lasting changes in the hypothalamic pituitary adrenal (HPA) axis reac-
tivity of the offspring (Sapolsky, Krey, & McEwen, 1984), as well as subsequent
behavioral impairment in coping under stressful conditions.
There is also evidence that suggests that prenatal stress effects may be medi-
ated by fetal serotonergic neurons. Rodent studies have demonstrated that mater-
nal stress significantly increased maternal plasma-free tryptophan and thereby
increased the amount of tryptophan available to fetal brains, resulting in elevated
serotonin levels in the fetal cerebral cortex (Peters, 1990). Finally, it has been
suggested that prenatal stress effects may operate via altered cerebral lateraliza-
tion. Fride and Weinstock (1988) attributed the increased level of anxiety noted in
prenatally stressed rats to a reduction in cerebral lateralization in the offspring as
538 SCHNEIDER

depicted by altered dopamine turnover rates in the right hemisphere in prenatally

stressed rodents.
Several limitations to the present study should be noted. First, one needs to
exercise caution in generalizing from the infant rhesus monkey model to the human
clinical condition. While the nonhuman primate model is a representation of the
human condition, it is not an exact replica (McKinney & Moran, 1979). Also, it is
important to note that there are wide individual differences in responsivity to
stressful life events among adults and infants (Suomi, 1987). Therefore, it is highly
unlikely that psychological disturbance would affect all mothers and their infants
in an identical manner. Finally, because the sex composition of the groups were
not identical, the gender findings should be interpreted cautiously. In future studies
it will be of interest to examine whether constitutional sources of individual differ-
ences, such as maternal temperament, mediate the effects of maternal exposure
to stressful events on the offspring. In addition, it will be important to discover
social or environmental postnatal conditions that can compensate for the apparent
alterations in behavioral expression resulting from maternal psychological distur-
bance during the prenatal period.

Notes
The author gratefully acknowledges the assistance of Elizabeth Roughton, Sara Rimm, and Sandra
Rogers in the data collection, of Christopher Coe and Susan Clarke for comments on a draft of this
manuscript, and of Maggie Kraak for help with preparation of the manuscript. This research was
supported by funding from the University of Wisconsin-Madison Graduate School and Department of
Therapeutic Sciences, The Maternal and Child Health Training Grant #9102, and the Intramural
Institute of Child Health and Human Development.

'Four groups (two from each prenatal condition) consisted of I female and 2 males. Two groups
(one from each prenatal condition) consisted of all females. The fourth control group consisted of all
males, whereas the fourth prenatal stress group consisted of 1 female and 2 males.
A 2 (Prenatal Condition) x 2 (Sex) x 9 (Behavior) between-subject MANOVA showed signifi-
cant ( p < .02) effects of prenatal condition, F(9, 12) = 3.68.

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