Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatta): developmental changes, behavioral stability, and early experience

INFANT

BEHAVIOR

AND

DEVELOPMENT

15,

155-l

77 (1992)

Neurobehavioral Assessment in Rhesus Monkey Neonates (Macacc~ muluffc~): Developmental Changes, Behavioral Stability, and Early Experience L. SCHNEIDER

MARY University

of Wisconsin-Madison

J. SUOMI

STEPHEN

National

Institute of Child Health and Human

Development

This prospective study documented developmental changes, individuol stability, and the effects of early experience on the neurobehoviorol repertoire of nursery-reared rhesus monkey neonates (Mococa mulatto) tested repeatedly across the first month of life. Thirty-six infants were tested three times weekly on o substantially modified version of the Neonatal Behavior01 Assessment Stole. The Infants were reared under several conditions in which their exposure to antmate ond inonimate obiects varied. Eleven infants were reared with only o cloth, 8 were reared with an upright cloth-covered surrogate, 7 were reored with on upright movable cloth-covered surrogate, and 10 were reored with an upright movable cloth-covered surrogote ond regular exposure to peers and novel toys. Infants reared with o movable surrogate demonstrated superior motor maturotion in comparison to those reared with only o cloth or cloth-covered surrogate. However, infonts reared with o movable surrogate OS well OS exposure to peers and novel toys showed not only greater motor maturotion than cloth-reored infants but olso greater responsiveness on orientation items and lower ratings of fearfulness when compared to infants in the three other conditions. Furthermore, the dato indicate that behovtorol stobility of individual differences con be demonstrated in indivrduols undergoing ropid developmental change regordless of rearing conditions.

Mococa

The

author

mulotfo neuromotor nursery

gratefully

rhesus maturity rearina

acknowledges

monkey

neonatal temperoment stabilitv individuol

the

assistance

enrichment behavior visual orienting differences

of Sara

McClurg. and Kirstcn Oleson in the data collection, Christopher Fcrguson for comments on a draft of this manuscript, and Joyce of the manuscript. This rcscarch was supported by the Graduate

Rimm.

Elizabeth

Roughton.

Suzy

Cot, Susan Clarke, and Sherri Zander for help with preparation School and the Department of

Therapeutic Science at the University of Wisconsin-Madison. the Intramural Research Program of the National Institute of Child Health and Human Development, and the Maternal and Child Health Training Grant No. Y 102. Corrcspondencc and rcqucsts for reprints should be sent to Mary L. Schneider, 2175 Medical Science

Center,

1300

University

Avcnuc.

Madison,

WI

53706. 155

156

SCHNEIDER

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SUOMI

There are a variety of reasons for studying neonatal behavior in nonhuman primates. These range from defining differences and similarities between human and nonhuman primates (Hallock, Worobey, & Self, 1989) to investigation of disorders common in human neonates and infants such as fetal alcohol syndrome (Clarren & Bowden, 1982), lead exposure (Levin, Schneider, Ferguson, Schantz, & Bowman, 1988), low birth weight (Gunderson, Grant-Webster, & Sackett, 1989), prenatal stress (Schneider, in press), and drug exposure (Golub, Sassenrath, & Chapman, 1981; Phillips & Lockard, 1985). In addition, the study of neonatal behavior in nonhuman primate infants can provide an avenue for investigating the effects of early environmental influences upon infant development under controlled conditions (Champoux, DiGregorio, Schneider, & Suomi, 1990; Schneider, Kraemer. & Suomi, 1991). Moreover, the experimental control possible in nonhuman primate studies enables the assessment of how such environmental influences may differentially affect certain infants based on their inherent behavioral style or temperament (Schneider, Moore, Suomi, & Champoux, 1991). Despite the extensive literature describing the effects of early experience on the behavioral development in nonhuman primates (see Mitchell, 1970, and Sackett, 1968, for reviews), to date there are only a few published reports on observations made during the neonatal period (Champoux et al., 1990; Schneider, Moore, et al., in press). Moreover, there are limited normative data pertaining to nonhuman primate neonatal development. The neonatal data that do exist are restricted largely to descriptions of motor development, for example, the dates of appearance and/or disappearance of reflexes (Caste11 & Sackett, 1973; Ehrlich, 1974; King, Fobes, & Fobes, 1974; Mowbray & Cadell, 1962; Sackett, Gunderson, & Baldwin, 1982). Using standard test protocols, investigators have also studied species variation in motor development, particularly in those infant reflexes that facilitate maternal contact (see Rogers, 1988, for a review). The predominant theme in behavioral research with human neonates is that human infants differ on temperamental characteristics (Kagan, 1982; Rothbart & Derryberry, 1981; Thomas, Chess, & Birch, 1968) and that these inherent temperamental qualities predict the kind of interaction the infant is likely to elicit from the environment (Brazelton, 1973). The Brazelton Newborn Behavioral Assessment Scale (NBAS) has been the most commonly used instrument for research with human neonates. Two studies have compared the behavior of chimpanzees and human neonates on the NBAS. Hallock et al. (1989) reported that, whereas human infants scored higher on an orientation cluster and lower in motor maturity relative to the chimpanzee infants, newborn chimpanzees were remarkably similar to human neonates in their behavioral responses on the NBAS. Similarly, Bard, Platzman, Lester, and Suomi (1992) reported striking similarities in early orientation ability between human neonates and nursery-reared chimpanzees.

NEUROBEHAVIORAL

ASSESSMENT

IN RHESUS

157

To provide detailed data on a wide range of neonatal behaviors, we developed an assessment instrument based on the NBAS to capture the characteristics and capabilities of the newborn rhesus monkey. This instrument was designed not only to specify the infants’ current behavioral responses pertaining to temperament, interactive, and neuromotor functioning but also to be used longitudinally to indicate emerging developmental trends. In this study, we report observations of the neurobehavioral repertoire of nursery-reared infants from birth through the first month of age who were reared under a number of conditions in which their exposure to animate and inanimate objects varied. We had three specific goals: (a) to describe changes in the emerging developmental functions, (b) to assess the behavioral stability of individual differences across time, and (c) to examine whether early measures varied as a function of environmental experience. METHOD

Subjects The subjects were 36 infant rhesus monkeys (Macaca mufutfa), 22 males and 14 females, who were tested from birth through the first month of age. All were vaginally delivered and healthy at birth. Birth weights for males ranged from 420 to 600 gms (M = 498, SE = 11.6); for females, the range was 415 to 605 gms (M = 510, SE = 14.3). Gestational age for males was 155 to 179 days (M = 169, SE = 1.5); for females, the range was 146 to 175 days (M = 169, SE = 2.1). Gestational age was assessed as the interval between the first day of the 3-day timed mating period of the mothers and parturition. All infants were separated from their mothers at birth and reared for the first 30 days postpartum in the laboratory nursing according to a standard procedure described by Ruppenthal (1979). Infants were nursery reared both to prevent confounding due to differential maternal treatment and to enable continuous access to the infants for testing. All subjects were individually housed in 41cm x 51-cm x 42-cm cages in visual, auditory, and olfactory contact with other infants during the first month of life. Subjects had free access to Similac infant formula (Ross Laboratories). There were four groups of infants born between April 1984, and June 1990. The first group consisted of 11 infants (9 males, 2 females) born in 1984, who were provided from birth with a cloth as a surrogate artificial mother and are referred to as cloth-reared. A second group of 8 infants (4 males, 4 females), 4 born in 1984 and 4 born in 1985, were reared with an upright cloth-covered stationary surrogate and are referred to as stationary-surrogate infants. A third group consisted of 7 infants (3 males, 4 females), 3 born in 1984 and 4 born in 1985, were reared from birth with an upright cloth-covered movable surrogate and a cloth-covered water-filled plastic pillow, and are referred to as movable-surrogate infants. The remaining 10 infants (6 males, 4 females), 6

158

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born in 1989 and 4 born in 1990, were reared from birth with a cloth-covered movable surrogate, a cloth-covered water-filled plastic pillow, two loops of plastic garden hose as a climbing apparatus, and a variety of brightly colored manipulatable infant toys rotated among infants daily. In addition, 4 days per week, they were socialized in dyads for 15 min. The latter infants are referred to as peer-toy infants. No differences across groups were detected for birth weight or gestation length. Infant Neurobehavioral Assessment Scale

A 20-min battery of developmental tests was administered on the following days postpartum: 4,6,8, 11, 15, l&22,25, and 29. Testing occurred between 10:00 a.m. and 12:00 p.m., approximately midway between feedings. The test battery was designed to assess a number of variables that mature across the first month of life. These variables fall into three categories: temperament, interactive, and neuromotor. Ratings were based on scales ranging from 0 to 2. The complete list of test items is given in Table 1. Observers were trained to reliability by the first author. Observers were not blind to the rearing condition of the infants; however, they were unaware of the experimental hypothesis being tested. The test began with the examiner wrapping the infant in a cloth diaper from the waist down, leaving the arms free to move. The orientation items were administered first. They consisted of ratings of the infants’ orienting and visual following responses elicited both to a plastic toy (Mickey Mouse face) and to a lipsmacking sound (simulating a monkey) made by the examiner. The percentage of time during which the infant was attentive was rated as well as the duration or length of the looks while orienting to the toy or sound. Neuromotor functions included ratings of muscle tonus, coordination, balance, tremulousness, response speed, and spontaneous motor activity. In addition, reflex items included righting reactions, grasp reflex, placing responses, rotation or tonic deviation of the head and eyes, rooting, the Moro response, and a measure of visuo-vestibular responses (Ayres, 1976). Muscle tonus was assessed while the infant was held in both the prone and supine positions and was based on the infant’s ability to maintain its head in a position against gravity. In addition, muscle tonus was assessed during both passive flexing and extending of the relaxed limbs, as well as while the infant was actively contracting its muscles. Temperament ratings were based on behaviors noted during the administration of the orienting and neuromotor items. The goal was to maintain the infant in a quiet, alert state throughout the administration of the sequence of items. Therefore, the infant’s temperament was constantly monitored and the examiner intervened to console the infant when appropriate. Ratings were subsequently made of numerous temperamental dimensions including response intensity, soothability, irritability, fearfulness, and distress to limitations (see Table 1 for further detail).

NEUROBEHAVIORAL

Definition

of Meosures

ASSESSMENT

IN RHESUS

TABLE I on Neurobehoviorol

159

Assessment

Items

Scale

Definition

Orientotion Visual

orientation

Eyes oriented toword positions in infont’s contact; 2 = direct

Visual

following

Eyes following moving object (plastic horizontol ond vertical directions (0 I = starts to follow; 2 = complete Exominer rating of length of looks on

Durotton

of looking

Attention

looking; Examiner ottention

span

attentive Stote

toy (plastic periphery prolonged

Mickey Mouse (0 = no orient; contact).

face) held I = direct

Mickey Mouse = contact but following). orlenting items

in foul brief

face) in both no following; (0 = no

1 = brief looks; 2 = I- to 2-s looks). roting of ottention on previous items (0 = lock of on oil items; 1 = ottenttve 25% of the time; 2 = 75%

of the time).

Control

Irritability

Amount

Consolobility

distress noted continuously; I = distress opparent 50% of examination; 2 = distress not opporent during the examlnotion) Eose of consoling infont during distress (0 = Impossible to soothe

Struggle

or console Infont; 1 = infant IS consoled with difficulty using holding, swoddling, rocking, and/or strokmg; 2 = infont wos eosy to console simply by picking up). Amount of squirming (0 = 25% of time squirming; I = infant

during

Predomlnont

Motor

testing state

of distress

noted

during

the entire

exominotion

(0 =

squirmed 50% of time; 2 = contmuous squirming noted.]. State of infont during exominotion (0 = alert, awoke, ond owore; 1 = alert but somewhot ogitoted; 2 = extremely agitated).

Maturity

Muscle

tonus-prone

Muscle tonus-supine Coordination Response

speed

Lobryinthion

righting

Ability to hold heod hanging

head up when held down; I = heod

prone lifted

(0 = flaccid tone but not mointolned

2 = head llfted and maintained for ot leost 3 s). Assessed exactly OS above but infont held I” supine Quality of movement roted (0 = clumsy movements;

with for 3 s;

position. 1 =

odequote movements, 2 = agile movements]. Exominer rating of speed of responding (0 = 25% of responses quick; I = 75% of responses qutck; 2 = 011 responses quick). Reolignment of head when body is tilted 45” sidewoys (0 = heod and lines

body in some plane; up with the vertical

Observotion

of motor

I = plone).

heod

portlolly

rights;

2 = head

Activity Motor

octtvity

Coordinotion

activity

during

o 5min

observotionol

(0 = motion 25% of the time; 1 = motion 50% continuous motion). Quality of movement roted (0 = clumsy movements; odequote movements; 2 = agile movements).

period

of the time;

2 =

1 =

(continued)

SCHNEIDER

160

TABLE

AND

SUOMI

1 (Continued) Definrtion

Items Locomotion

Quality of locomotion 2 = coordinated

Possrvity

Duration time;

Individual

of time spent inactive (0 = none; 2 = Inactive 75% or more).

I = weak

and

grasp

Auditory

startle

Auditory

orient

Tactrle

Attempts

1 = inoctrve

50%

of the

and

grosp

Response to tactile (0 = no response; definite curvation

plantor

Response grasping; voluntary

response righting

Visuo-vestibular

orient/follow

toy

(0 = no attempt;

stimulus lateral 1 = barely noted).

to examiner’s 1 = portiol release).

and parallel to vertebral column apparent curvatron of spine; 2 =

index finger placed grasp; 2 = strong

rn palm reflexive

response

Tremulousness

vocalizations extremely Duration and excursion rotation (lo/20 s) on

loud length rotary

Self-mouth

Infant’s behavior when placed in on enclosed calm 90% of time; 1 = calm 50% of time; distress). manipulatrons

mild

and/or shrill in expression). of postrotary nystagmus following board (0 = for no observable 2 = for of nystogmus

Examiner ratrng of tremulousness (0 = no incidents; incrdents, 2 = 3-4 incidents). Number of vocalizations in o 1-min trme period.

Vocalization Self-quieting

Fearfulness

(0 = no reflex grasp without

resistance to supine position with attempts to turn over). Examiner rating of quality of vocal reactions (0 = vocalizations in intensity; 1 = vocalizations moderote or average, 2 =

intensity

nystagmus; 1 = for barely apparent nystagmus; nystagmus 1 mm or greater in length). Duration seconds was recorded in both directions.

motor

1 =

Time noted for infant to turn from supme to prone (0 = portral righting; 1 = nghts in 5 to 15 s; 2 = rights in less than 5 s). Infant IS pulled from supine to sitting (0 = limbs extend and heod lags; 1 = arms moderotely flexed with no heod lag; 2 =

Pull-to-sit

Response

vrsual

mode rn infant’s periphery (0 = no orientmg; I = partial headturning; 2 = full head-turn with visual inspection of source). Response to tactile stimulus to four extremities (0 = no response; 1 = barely discernible response; 2 = easily apparent response).

response

Palmar

to grasp

gross swat; 2 = intentional grasp with finger flexion). Response to sudden noise (0 = no response; 1 = eye blink and/or head ierk; 2 = body terk). Eyes oriented toward lipsmacking noise srmulating monkey sound

response

Galont’s

Fine

attempt;

Items

Reach

Body

was roted (0 = none; locomotion noted).

1 =

in

l-2

area for 5 min 2 = continuous

(0 =

Durotion of time engoged in fine motor activities in observational period (0 = none, I = less thon 5 s, 2 = more than 5 s). Fear grimaces or trembling (0 = none; 1 = feor grimaces early testing session; 2 = fear noted frequently). Inserting hands 2 = insertion

or feet lasted

in mouth (0 = none; 15 s or more).

1 = brief

insertion;

(continued)

in

NEUROBEHAVIORAL

ASSESSMENT

TABLE

1 (Conttnued)

Items

Definition

Mointenonce

of balance

Possive range of motion (muscle tonus) Active

Placing

Infant

is held

in the sitting

position

and

support

is withdrawn

(0 =

infant falls over; 1 = places hands out but falls; 2 = uses hands for support and maintoins balance]. Degree of resistance to passive flexion and extension of limbs (0 = barely discernible resistance; 1 = moderate resistance; 2 = strong resistance). Strength of muscles when actively contracting (0 = some strength but connot withstand slight resistance; 1 = withstands moderate

power

resistance; 2 = extremely Infant places foot or hand darsum of hand or foot definite response).

response

Parachute

response

Rotation (tonic of heod and Moro

161

IN RHESUS

deviotion eyes]

reflex

Distress

to limitations

Rooting

reflex

strong) on surface following tactile stimulus (0 = absent; I = weak response;

to 2 =

Upper extremity limb extension following head-first descent toward surface (0 = no orm extension; 1 = partial extension and openmg of the honds; 2 = definite orm extenston with open hands). Degree to which rotation, both weak Degree flexion

head and/or eyes with head free and

turn into restroined

the

dlrection of (0 = obsent; 1 =

turn; 2 = definite response). of abduction and extension in upper extremities following of head ond sudden withdrawal of support while supine

(0 = none observable; 1 = 45” of abduction, 2 = 90” or more of abduction). Infant’s movement was restricted for 10 s and degree of squirming was noted (0 = resistance 25% of the time; 2 = resistance 50% of the time; 3 = constant resistonce). Infont’s response (head-turning toward stimulus at the corner of the mouth turn toward stimulus; 2 = full turn].

stimulus) (0 = no

to light response;

tactile 1 = ihreak

Data Analysis

Separate analyses of variance were computed with years as the betweensubjects variable and days of testing as the repeated measure for the stationary-surrogate (1984 vs. 1985), movable-surrogate (1984 vs. 1985), and peer-toy (1989 vs. 1990) infants. Because there were no significant differences across years, subjects from similar rearing conditions were combined across years for subsequent analyses. To determine if there were significant effects for rearing condition and days of testing, all measures were evaluated using mixed-design analyses of variance (ANOVA) with rearing condition as the between-subjects variable and days of testing as the repeated measure. When an overall F was significant for rearing condition, the Fisher test was used to compare all possible pairs of

162

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treatment means (Keppel, 1982). Correlational analysis was used to test the stability of performance over time. Linear trend analyses were performed to assess whether the best-fitting linear function for the four groups differed. The slopes of the best-fitting functions were computed for each subject by taking the sum of the cross products of the scores multiplied by the linear coefficients of orthogonal polynomials. ANOVAs were performed with groups as a between-subjects factor. Similar procedures were repeated using the quadratic coefficients of orthogonal polynomials to assess whether the best-fitting quadratic functions differed across groups. Analyses were performed on individual measures as well as on composite scores. Composite scores were based on prior factor analyses described by Schneider, Moore, et al. (in press). These consisted of four composite scores: orientation, state control, motor maturity, and activity. The orientation score was composed of visual orienting, visual following, duration of looking, and attention span. State control consisted of irritability, consolability, struggle during testing, and predominant state. Motor maturity was composed of muscle tonus-prone, muscle tonus-supine, coordination, response speed, and labyrinthian righting. Finally, activity was composed of motor activity, coordination, locomotion, and passivity (see items defined in Table 1). All measures were examined for sex differences using ANOVA (sex by days of testing), and none was found. RESULTS Developmental Change

Developmental changes across the first month of life were examined using ANOVA with days of testing as the repeated measure (see Table 2, pp. 164165). The infants’ scores increased with age on orientation, F(8,256) = 8.22, p < .OOl, on motor maturity, F(8, 256) = 12.22, p < .OOOl, and on activity, F(8,256) = 22.11, p < .OOOl, composite scores. Along similar lines, analyses of individual items demonstrated significant (all ps < .05) increases with age on individual orienting items (visual orienting. visual following, reach and grasp, duration of looking, and attention span), significant increases in neuromotor capabilities (muscle tonus, body righting, pull-to-sit, response speed, motor activity, coordination, locomotion, balance, muscle tonus while passive, active power, and parachute response), and significant decreases in the primitive reflexes (moro, rooting, and grasping) across testing session (see Table 2 for details). Within the domain of temperament, ratings of response intensity, fearfulness, and distress to limitation increased significantly with age. Finally, both auditory orienting and visuo-vestibular responsivity decreased significantly with age. Stability Across Testing Sessions. Stability was summarized in two ways: (a) at 3- to 5-day intervals between tests, and (b) at l- to 3-week intervals

NEUROBEHAVIORAL

ASSESSMENT

IN RHESUS

163

between tests. The 3- to 5-day interval data provide a detailed picture of patterns of stability and instability during the neonatal period. The I- to 3-week interval data provide a picture of long-term neonatal continuity. Table 3 (pp. 166-167) shows the correlations across the first month of life at 3to 5-day intervals between tests. As can be seen in Table 3, overall, the correlations were moderate to highly significant. In fact, orientation, motor maturity, and activity composite scores were all significantly correlated across the 9 testing days from the first day of testing. State control, on the other hand, showed stability only from Day 12 postpartum. Examination of individual items also revealed moderate stability across the first month of life for the majority of items (see Table 3 for details). Table 4 (p. 168) shows correlations at l- to 3-week intervals. For Days 6 to 15, measures of motor maturity showed reliable continuity, all rs < .05. These included the motor maturity composite score, activity composite score, muscle tonus-supine, locomotion, coordination, balance, parachute reaction, tremulousness, and visuo-vestibular responses. Correlations from Day 15 to Day 29 improved slightly over the 6- to 15-day interval. Motor maturity and activity measures continued to show stability. These included the motor maturity composite score, activity composite score, muscle tonus-prone, motor activity, coordination, placing, tremulousness, and visuo-vestibular responses. Moreover, orientation items began to emerge as reliable indices, with the orientation composite score and duration of looking showing reliable continuity. Finally, analysis of correlations between Days 6 and 29 revealed little agreement between test scores. Rearing Eflecrs. Comparison of the four rearing conditions indicates that there was an overall significant rearing effect for the orientation composite score across groups of infants, F(3,32) = 5.73, p < .003 (see Figure 1, p. 169). Post-hoc testing revealed that the peer-toy group showed significantly greater responsiveness to the orientation items when compared to the cloth-reared, stationary-surrogate, and moving-surrogate groups, all ps < .05. Moreover, linear and quadratic trend analysis revealed differences in the linear component, F(3, 32) = 3.03, p < .05, across groups with the peer-toy group demonstrating a steeper slope. There were no group differences on orientation for the quadratic component. In addition, an inspection of the means for the individual items in the orientation grouping showed significant differences across rearing conditions for visual orient, F(3,32) = 10.15, p < .OOOl, visual follow, F(3,32) = 10.07, p < .OOOl, and for reach and grasp, F(3,32) = 3.40, p < .05 (see Figure 2, p. 170). Post-hoc testing revealed that the peer-toy infants were significantly more responsive than the cloth-reared, stationarysurrogate, and moving-surrogate infants, all ps < .05, on these three measures. Linear trends were also significantly different across groups for visual orient, F(3, 32) = 4.36, p < .Ol, visual follow, F(3,32) = 6.47, p < .OOl, and reach and grasp, F(3, 32) = 3.00. p < .05.

and

of look span response response grosp grasp tonus-prone

Reach Auditory Auditory Duration Attention Tactile Galont Polmar Plantor Muscle

Response

speed

Muscle tonus-supine Body righting Pull-to-sit Labyrinthian righting

grasp startle orient

orientation follow

Measures

Visuol Visual

lndividuol

1.29 1.56 1.00 0.82 0.93

0.59 0.96

1.34 0.76 0.60 1.31

1.16 0.86 1.19

0.49 0.86 I .65

0.41 0.40

0.57 0.75

0.71 0.98

6

Scares

1.31 1.69 0.89

0.94 1.13 1 .oo 1.46

0.99 0.67 0.91

0.25 0.75 1.65

0.24 0.23

0.55 0.66

State control Activity

4 0.52 0.91

Scores

Orientation Motor maturity

Composite

Mean

far

0.75 0.78 0.74 0.82 1.39 1.32 1.08 1.10 1.31 0.65 0.70 1.59 1.49 i .a7 1.18 0.71 1.01

0.78 0.67 0.95 0.76 1.61 1.35 1.04 1.13 1.25 0.71 0.54 1.42 1.32 1.65 1.04 0.63 0.99

0.68 1.13

1.17

1.Ol 0.62 0.92

12 0.98

a 0.95

Days

Neurobehaviorol Postpartum

1.81 1.51 0.92 1.01

1.60 1.64

1.24 1.06 1.40 0.41 0.27

0.78 1.10 i .4a

0.81 1.oo 1.oo

0.69 1.34

1.31

1.15

15

2

18

1.31

1.17

I .a9 1.44 0.48 . 1.11

1.78 1.76

1.31 1.05 1.42 0.27 0.30

0.78 1.34 1.50

0.95 0.92 1 .oo

0.81 1.34

Measures

TABLE

1.90 1.51 0.64 1.18

1.69 1.42

1.22 1.29 1.19 0.10 0.18

0.86 1.04 1.51

0.95 1.60 0.83

0.68 1.40

1.29

1.15

22

Across

1.97 1.65 0.85 1.17

1.64 1.43

1.20 1.26 1.12 0.05 0.19

0.66 0.68 1.57

1.10 1.60 0.97

0.75 1.41

1.34

1.21

25

First Month

2.00 1.60 0.75 1.32

1.77 1.40

1.29 1.10 1.08 0.11 0.11

0.62 0.68 1.56

1.10 1.50 1.10

0.79 1.46

1.37

1.19

29

of Life Significant

n.s. ns. n.s. n.s.

I

l

n.s *

tt*

l **

t* tt

*** l *

***

ns.

et*

*t*

n.s.

ns. n.s. n.s. n.s.

l **

n.s.

l **

***

ns. ns. ns.

l ** ***

n.s ***

***

*t*

Da&’

l **

n.s. ns.

***

**

Effects Rearing Condition”

Response

limitation

0.49

0.50 1.28 1.78 0.57 0.61

1.42 1.17 1.17

0.94 0.75 0.61

0.99 0.42 0.64

1.32 1.78 1.35

0.69 12.44 0.64 0.90

1.07 1.47 13.61

df = 8, 256.

df = 3, 32

0.81

1.07 1.74 0.58 0.49

0.94 1.65 0.67 0.54 0.88

0.94 1.03 0.83

1.06 0.79 0.57 1.15

0.99 0.36 0.71

0.89 1.53 1.30

7.33 0.44 0.79

1.68 16.07 0.51

1.10

0.85 1.10 1.04 0.76

1 .oo 0.68 0.57

0.87 0.36 0.50

0.69 1.26 1.09

8.39 0.50 0.61

1.67 17.54 0.68

0.78

rearing condition: days of testing: lower possiwty p < ,001.

0.51 1.19

0.89 0.82 1.75 0.92

0.89 0.60 1.75 1.08 0.39 1.33

0.78 0.89 1.01

0.44 0.93 0.93

0.73 0.66 0.50

0.84 0.28 0.34

0.85 0.19 0.28 0.53 0.69 0.49

0.43 0.89 1.29

0.82 7.25 0.33 0.44

0.78 9.92 0.49 0.29 0.18 0.78 1.40

1.02 1.76 19.39

0.92 1.64 19.06

0 Effects are significant for b Effects are significant for ’ Higher score represents l p < .05. ** p < .Ol. ***

Rooting

Ratotion Moro Distress

Balance Possive ROM Active power Placing Parachute

Self-mouth Struggle Predominant

Consolability Fearfulness

Coordination Locomotion Passivity Irritability

Vocalization Self-quieting Motor activity

state

intensity

VOR excursion VOR duration Tremulousness

0.64 0.34

0.78 1.35 1.67 0.58

1.56 1.31 1.39

1.22 1.06 0.60

1.39 1.14 0.46 0.67

0.81 1.43 1.74

0.53 6.28 0.36

1.11 1.53 13.92

0.60 0.81 0.50

0.87 1.31 1.68

1.62 1.28 1.21

1.08 0.64 0.60

1 .Ol 0.46 0.56

0.90 1.49 1.81 1.42

0.72 7.81 0.31

1.07 1.56 14.37

0.40 0.83 0.37

0.77 1.49 1.67

1.59 1.37 1.33

0.69 0.86 0.83 0.67

1.51 1.07 0.44

0.81 1.56 1.75

0.51 13.22 0.47

1.12 1.46 14.37

0.69 0.81 0.18

0.68 1.51 1.57

1.69 1.33 1.31

1.14 0.92 0.65

1.83 1.41 1.06 0.54 1.12

0.64 0.93 1.64

0.60 16.83

1.67 14.43

1.28

n.5.

**

l

ns. n.5. II

ns. n.s.

n.s. n.s. n.s. **

n.s. n.s. *

n.s. n.s.

tt*

t**

l **

n.s.

l **

n.s.

l *t

***

l **

n.5. n.s.

n.s. n.s. ns. *** *t*

n.s. *** *** *** n.5. *

l * **

*

n.s. It

*.*

l *

n.s.

n.s. n.s. n.s.

Scores”

ond

span response response grosp grasp tonus-prone

Reach Auditory Auditory Duration Attention Tactile Golont Polmor Plontor Muscle Muscle tonus-supine Body righting Pull-to-sit Lobyrinthion righting

grosp stortle orient of looking

orient follow

Measures

Visual Visual

Individual

Motor maturity Stote control Activity

Orientotion

Composite

Correlations

14 .03 .15 .22

.38* .60* .35* .60***

.41* .24 .17

.45** .42* .44** .29

.47” .52** .42’ .42’ - .07 - .09 .40*

.06 09 .05

.24 .48”

.47** .40’ .42* .68*”

6-8

.23 .44” .26

.38* .42*

.58”’ .63’*’ - .09 .64***

4-6

for Neurobehoviorol

Measures

.52* .68*** .20 .I5 .33* .30 .35’ .04

.17 42’ .lO .36’ .34’ .28 .43** .27 .21 .43** .33* .67”’ .13 .36’ .14

.45** .l 1 .09 .22 .57”’

.27 .45** .33’ .54***

.26 .I3

.31

37’

.53*** ,431”

.50** .62”’ .43** .64”’

15-18

Postpartum

Month

.41* -30 .l 1

.37’

.39*

12-15

Days

the First

.33* .42’ .55”’

3

.42* .34’ .14

%12

TABLE Across of Life

-

.34* .ll .04 .24 .32

.31 .07 .29

.48” .33* .52** .55***

.28 .35* .54”’ .43** .02 .55***

.05 .44** .51”

.I6 .67”’ .19

.oo .41’ .20

.15 .11

.42’ .36’ .53*** .34*

.ll .13 .63***

.24 .61**’ .I1

.63**’

.56**’ .54”’

.60**’ .70***

.62”*

.51** .51”

25-29

.53*** .64”*

22-25

mtervols)

.23 .35* .16

.29 .42* .15

.39*

.43** .37* .52**

.31

18-22

(3- to 5doy

“df = 34. * p < .05. ** p < .Ol.

Response speed Response intensity VOR excursion VOR duration Tremulousness Vocalization Self-quieting Motor activity Coordination Locomotion Passive Irritability Consolobility Fearfulness Self-mouth Struggle Predominant stote Balance Passive ROM Active power Placing Porochute Rotation Moro Distress limitations Rooting

l

** p < ,001

.48** .48** .33' .75*** .16 .25 .I5 .23 .67"* .44** .69*** .12 .24 .51** .36 .29 .13 .50* .64*'* .59*** .17 .49** .19 .80*** -42' .49**

.08 .51** .lO .45** .40 .39' .19 .56*" .44** .39* .49" .27 .51** .37' .14 .30 .59*** .27 .13 ,668" .03 .74"' .09 .67"' .I2 .32

.17 .34* .29 .63*" .33* .28 .38' .27 .19 .59*** .34* .34* .12 .Ol .42* .02 .18 .36* .38* .51* .09 -44" .04 .43** .07 .43** .35* .61**' .37' .68*'* .53*** .33* .48** .37* .36* .08 .36* .54"' .53*** .24 .56*'* .41 .34' .31 .43** .41* .49** .59*** .26 .44** .32 .22

.53*** .51** .28 .51*** .25 .42* .I9 .45** .52** .51** .47** .40* .23 .32 .55*** .42 .32 .54*** .21 .lO .49** .72'** .32 .55*** .28 .31

.31 .39* .30 .58'*' .25 .44** .28 .71*** .48*' .l 1 .28 .lO .32 p.02 .55*** .41 .37' .21 .27 .27 .40* .17 -.05 .50** .34* .37*

.52** .34* .17 .56"* .47.I7 .41* .73"' .61*** .52** .67'** .29 .41* .51** .50* .43 .55*** .49* .76"' .58*** .66*'* .52** .30 .82"' .41* .46**

.25 .46** .35* .46** .50** .42* .26 .60*** .61*** .15 .26 .48** .49** .39* .74*** .61 .38' .57-* .41* .47** .32 .31 .53** .62*" .54*** .53***

Correlotions

TABLE 4 Measures

for Neurobehaviorol

(1. to 3-week Davs

Composite

Scores”

6-15

.oo

Orientation Motor maturity State control

/57*** - .22

Activity Individual

15-29 .38* .43” .20

.47”

.35*

&29 -.ll .09 .05 .34’

Measures

Visual Visual

orientation follow

.lO -.Ol

.21 .14

Reach Auditory Auditory Duration

and

.29 .23 - .23

.32 .32 .oo

Attention Tactile Gafont

span response response

.02 -.14 .21

.43** .31 .34*

Polmor Plontar Muscle

grosp grasp tonus-prone

.35* .18 .05

.lO .lO -.13 .33*

grasp startle orient of look

.15 .37* .14 .25

Muscle tonus-supine Body righting Pull-to-sit Labyrinthion righting Response speed Response intensity VOR excursion VOR duration Tremulousness Vocolizotion Self-quieting

Fearfulness Self-mouth Struggle Predominant Balance

.13 .29 .20

.19 .59*** .34*

.34* .52** .35*

.34* .48** .27 - .20 -.ll

Passivity Irritability Consolability

.Ol .43” .03 -.14 .33* .13

stote

Possive ROM Active power Placing Parachute

- .09 - .04 .53*** .23 .32 .30

limitations

“df = 34. l p < .05. ** p < .Ol.

***

p < ,001.

.20 .oo - ,004

.32 .20 .OB

- .OB - .04 .30

Motor activity Coordinotion Locomotion

Rototion Distress Rooting

intervals)

Postoortum

.14 .20 .36* .41* -.14 .39’ .13 .20 - .08 .42**

.07 .08 .02 .22 .lO - .06 - .33* .06 .02 .12 .17 .oo .02

.J3 - .07 - .32 - .20 .15 .23 .17 -.ll .28 .26 .36’ .32 .03 .ll .07 .18 .25

.34** .oo .06

.15 .02 .20 .23

.13 - .05 .33* .30

- .20 .25 .03 .30

.02 .09 .09

- .25 .24 .15

NEUROBEHAVIORAL

ASSESSMENT

169

IN RHESUS

2.0 uz v)

1.8 1.6 -

z E .-

1.4 -

r2

1.2 -

tz

1.0 -

5

0.8 -

iis

0.6 -

64

0.4 -

c

;j 0

V * M

Cloth Sfationaw Movable. Peers/toys

,

,

(

,

,

,

,

4

8

12

16

20

24

28

Days Postpartum Figure

1. Mean

scores

on orientotion

across

first month

of life as o function

of rearing

condition.

Likewise, comparison of means on the motor maturity composite score revealed a significant overall effect of rearing conditions, F(3,32) = 7.54, p < .0006 (see Figure 3, p. 171). The peer-toy infants demonstrated an advantage in motor maturity when compared to the cloth-reared and stationary-reared infants, but not in comparison to the moving-surrogate infants. Furthermore, there was a significant difference for motor maturity between the movingsurrogate and stationary-surrogate infants. Inspection of the scores that compose the motor maturity composite score revealed significant differences across groups for coordination, F(3, 32) = 3.13, p < .04, muscle tonussupine, F(3,32) = 5.84, p < .003, and muscle tonus-prone, F(3,32) = 5.72, p < .003 (see Figure 4, p. 172). For coordination, there was significant advantage for the peer-toy group over the cloth-reared group. For muscle tonus-supine, there was a significant advantage for the peer-toy infants over the cloth-reared and the stationary-reared infants. In addition, the infants reared in the movable-surrogate condition were superior to those reared in the stationary-surrogate condition. For muscle tonus-prone, both the peertoy infants and the movable-surrogate infants were superior to the clothreared infants, all ps < .05. Linear and quadratic trend analysis revealed no significant differences across groups.

170

SCHNEIDER

AND

20 _ T I

Visual Cloth Slstionwy Movable

‘S-

PeeKKoys

-

SUOMl

Orient

1.0 -

0.5 -

0.0

0

I 0

I 16

Visual

0.0

! 0

I 8

1 24

Follow

I 16

Reach

and

24

Grasp

2.0,

I 0

1 16

Days Figure across

2. Mean scores on visual orient first month of life as o function

24

Postpartum

(upper), v~suol follow of rearing condition.

(middle),

and

reach

and

grosp

(lower)

NEUROBEHAVIORAL

ASSESSMENT

171

IN RHESUS

2.0 s! E ul

z 5 .-

1.8 1.6 1.4

c2

1.2

m”

1.0

5

0.8

z 5

0.6

:

L_ + * V

0.4 2

Cloth Stationary Movable Peers/toys

0.2

s 0.0 0

I 4

I 0

1 12

I 16

I 20

I 24

I 28

Days Postpartum Figure

3. Mean

scores

on motor

maturity

across

first month

of life OS o function

of reoring

condition.

In addition to the effects on the composite scores, infants were found to differ across rearing conditions in self-quieting, F(3, 32) = 5.92, p < .003, fearfulness during testing. F(3, 32) = 2.94, p < .05, balance, F(3, 32) = 13.64, p < .OOOl, distress to limitations, F(3, 32) = 4.08, p < .02, vocalizations, F(3, 32) = 4.19, p < .02, rotation reflex, F(3,32) = 2.92, p < .05, and moro reflex, F(3, 32) = 9.38, p < .05. The peer-toy infants were rated as superior in self-quieting, lower in fearfulness, superior in balance, higher in distress to limitations, emitted fewer vocalizations in a novel environment; they demonstrated a lower level of rotation or tonic deviation of head and eyes and an attenuated moro response when compared to the infants reared without early exposure to peers and toys. DISCUSSION This prospective study documents developmental changes, individual stability, and effects of environmental experience in nursery-reared rhesus monkey infants tested repeatedly from birth through the first month of age. The overall finding that the large majority of the infants’ responses changed significantly with age was not surprising. Clinically and intuitively, these results make sense, in that one would expect the infants’ orientation to visual stimuli, their neuromotor capabilities, and their activity level to increase

172

SCHNEIDER

AND

SUOMI

Coordination 20-

1.5-

l.O-

ClOlh Stationary MOWble

0.5 PWdTOYS

Muscle

0.0

! 0

Tonus-Supine

I 0

I 16

Muscle

Tonus-Prone

I 24

20

1.5

1.0 :

0.01 0

8

Days Figure prone

16

24

Postpartum

4. Mean scares on coordination (upper), muscle tonus-supine (middle), (lower) across first month of life as a function of reoring condition.

and

muscle

tonus-

NEUROBEHAVIORAL

ASSESSMENT

IN RHESUS

173

rapidly across the first month of life. Prior studies have documented increases in gross motor skills, including locomotion and climbing, decreases in the presence of early primitive reflexes, such as rooting and grasping, and increases in visual orienting behaviors with age (see Rogers, 1988, for a review). However, the present study is unique in that it expands upon prior work to provide normative data on a number of variables emphasized in the human literature, yet ignored in other studies on nonhuman primates (e.g., muscle tonus, righting reactions, and a variety of temperamental characteristics). The data on individual behavioral stability over time parallel reports on human children (Honzik, 1976) that indicate that correlation coefficients vary widely depending on the particular measure at hand, the size of the interval between tests, and the age of the subjects at the time of testing. The correlations across 3- to 5-day intervals in the present study were moderately high for most of the measures. This finding was interesting given the lack of day-today stability over the first few weeks of life reported for human neonates (Sameroff, 1978). There are several potential explanations for these findings. First, the nursery-rearing condition permitted all subjects to be reared under identical conditions in terms of housing, lighting, nutrition, and caregiver contact. This is in direct contrast to studies with human neonates in which these factors are subject to wide variance across subjects. Second, because rhesus monkey neonates are born in a more mature state than that noted with human neonates, especially with regard to motor maturity, they may indeed have greater behavioral stability than human neonates. Third, the structure of our procedure differs from that typically used in human neonatal studies (Brazelton, 1973), in which the sequence of test items varies based on the responses of the infant. In our procedure, infants were presented with an invariant sequence; the use of a standard procedure might have enhanced our finding of increased behavioral stability across testing sessions. It should be noted that, whereas the nursery-rearing condition controls for potential differences in maternal care, nursery rearing produces dramatic effects on early behavioral ontogeny and on the activity of brain biogenic amine systems (Kraemer, Ebert, Schmidt, & McKinney, 1989). This limits direct generalization of these data to rhesus monkey infants reared in species-typical environments. The finding that stability coefficients for l- to 3-week intervals were lower than those found for 3- to 5-day intervals is consistent with reports on human children that correlations decline as the time span between tests lengthens (Honzik, 1976). Correlations between Days 6 and 15 were only significant for motor maturity and activity composite scores, muscle tonus, tremulousness, coordination, and locomotion. Similarly, correlations from Day 15 to Day 29 were significant for measures of motor maturity and activity; however, orientation and duration of looking were also stable during this interval. The finding that orientation items showed stability only from Day 15 on was not

174

SCHNEIDER

AND

SUOMI

surprising given that nursery-reared rhesus monkey neonates were found to visually orient and follow an object only during the second week of life; hence, one would not expect to obtain reliable measurements of this function prior to 15 days of age. Lastly, there was poor agreement between assessments performed at 6 days of life and 29 days of life. Several conclusions can be made from these data. First, as with the human data, the smaller the interval between testing, the better the correlations. Second, the grouping of test items a priori into motor maturity, activity, state control, and orientation composite scores has apparently served to improve correlations. Third, the specific nature of the measure and the time of testing is important. For example, observations of items related to motor maturity and activity appear to be more stable during the early neonatal period in hand-reared rhesus monkey infants. Orientation items, emerging later in the neonatal period, only show stability from Day 15 postpartum on. Finally, as with human neonates, when one takes two measurements that span a time period that involves rapid developmental changes within the individual, one is not apt to obtain satisfactory measures of continuity. Therefore, some researchers (Wohlwill, 1973) have advocated the need for repeated assessments across time in order to plot a developmental curve. Continuities as well as discontinuities then become windows into the developing systems (Brazelton, . 1990). The finding that infants reared in the toy-peer condition had significantly higher orienting scores, better motor maturity scores, and lower ratings on the dimension of fearfulness compared to nursery-reared infants without exposure to peers and novel toys requires some comment. Because we had tested the neonate repeatedly, we were able not only to determine that infants in the peer-toy condition were better on visual orienting, visual following, and reach and grasp but also to conclude that the slope of the bestfitting line was steeper for the peer-toy infants on these items. These data illustrate the usefulness of implementing repeated testing in order to express data in terms of developmental functions. Furthermore, these comparisons of infants reared under different nurseryrearing conditions demonstrate that the nursery environment can have striking consequences even at a very early age. While the effects of environmental experience have been extensively documented in nonhuman primates (see Mason & Berkson, 1975; Sackett, 1968, for reviews), the present study is one of the few studies to describe effects expressed during the first few weeks of life. These data underscore the benefits of early exposure to social and nonsocial stimuli in nonhuman primate studies in which the experimental design requires nursery rearing to decrease differential maternal treatment and to enable the investigator repeated access to the infants for testing. Further investigation is needed to explore whether these data will generalize the infants reared in species-typical environment, that is, with maternal and peer contact.

NEUROBEHAVIORAL

ASSESSMENT

IN RHESUS

175

Caution is warranted regarding generalization of these data for human infants. One might be tempted to liken the nursery-rearing state in the present study to the condition in which human infants are reared in neonatal intensive care units (NICU). However, it is important to note that the rhesus monkey neonates in the present study were healthy normal infants, whereas occupants of NICUs either have documented handicaps or have experienced potentially brain-injurious events associated with long-term developmental sequelae. Whereas supplementary stimulation was beneficial to the normal nursery-reared monkeys in the present study, one cannot assume that such stimuli would benefit human infants in NICUs. In fact, high-risk infants can tolerate only limited amounts of handling or stimulation due to problems with temperature regulation and stress tolerance (Anderson, 1986). Furthermore, it is not certain whether these data would generalize to healthy human newborns given that human neonates are significantly less mature during the first month of life when compared to macaques. Taken as a whole, our data illustrate that it is possible to measure neurobehavioral development in normal healthy nursery-reared rhesus monkey infants during the first month of life using instruments adapted directly from tests typically used with human neonates. Furthermore, individual behavioral stability was demonstrated, despite the finding that the infants were undergoing rapid developmental change across the first month of life. However, the degree of stability depended on the age of the infant when tested, the size of the time interval between tests, and the particular nature of the function measured. Two points spaced widely across the neonatal period were not particularly useful, whereas repeated measurements characterizing the shape of the developmental function as well as the periods of stability and instability are promising. Finally, our data demonstrate that the early nursery experience can alter an infant’s performance on neonatal measures, particularly on those pertaining to motor maturity and orientation. REFERENCES Anderson, Ayres,

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Wohlwill,

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C.F.. Suomi. environmental

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development. 21 November

New

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Academic.

1990; Revised

20 May

1991

W