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Temperament is an individual’s nature and is widely believed to have a heritable foundation. Few studies, however, have evaluated paternal and maternal contributions to the triadic dimensions of temperament. Rhesus monkeys are widely utilized to model genetic contributions to human development due to their close genetic-relatedness and common temperament structure, providing a powerful translational model for investigating paternal and maternal genetic influences on temperament. The temperament of rhesus monkey infants born to 19 different sires and 50 different dams was assessed during the first month of life by comparing the temperament of paternal or maternal half-siblings reared with their mothers in species-normative conditions or reared in a neonatal nursery. Factor scores from three dimensions of temperament were obtained (Orienting/Regulation, Negative Affectivity, and Surgency/Extraversion) and ANOVAs were used to assess genetic effects. For paternal half-siblings, results showed a statistically significant paternal contribution to Orienting/Regulation, Negative Affectivity, and Surgency/Extraversion factor scores. For maternal half-siblings, results showed a statistically significant contribution to Orienting/Regulation factor scores. When parsed by early rearing condition, results showed a paternal contribution Orienting/Regulation, Negative Affectivity, and Surgency/Extraversion scores for paternal half-siblings reared in the neonatal nursery, while there was only a paternal contribution to Surgency/Extraversion for paternal half-siblings reared by their mothers. There was only a maternal contribution to Orienting/Regulation for maternal half-siblings reared by their mothers. These results show that paternal and maternal contributions to temperament vary by environmental context, and that mothers may environmentally buffer their infants from paternal contributions to their temperament.

Attempts to describe the latent structure of human infant temperament have led some to suggest the existence of three major dimensions. An earlier exploratory factor analysis (EFA) supported a triadic structure of temperament in week-old rhesus monkey infants, paralleling the structure in human infants. This study sought to confirm the latent triadic structure of temperament across the first month of life in a larger sample of rhesus monkey infants (N = 668), reared by their mothers or in a neonatal nursery. A weekly behavioral assessment was obtained during the first month of life using a subset of items from the widely utilized Infant Behavioral Assessment Scale (IBAS), an instrument designed to measure temperament in infant monkeys. Using the latent constructs proposed by the earlier EFA (Orienting/Regulation, Negative Affectivity, Surgency/Extraversion), multi-group, multi-time point confirmatory factor analyses were conducted to confirm the latent temperament structure across rearing groups at each time point (weeks 1-4). Results confirm and extend those of the earlier EFA: latent Orienting/Regulation, Negative Affectivity, and Surgency/Extraversion constructs were present across the rearing groups at each time point, with the IBAS items consistently loading onto the latent factors to a similar degree across rearing groups at each time point. These findings suggest foundational evolutionary roots for the triadic structure of human infant temperament, but that its behavioral manifestations vary across maturation and rearing condition. Similarities in latent temperament structure in humans and a representative nonhuman primate highlights the potential for utilizing translational nonhuman primate models to increase understanding of human temperament.

This longitudinal study spans two generations of rhesus monkeys. First, the study investigates the effects of early rearing experiences on the maternal behavior of first-generation mothers (rates of premature infant rejection) and, second, the study investigates the effects of maternal rejection on the behavior of second-generation infants. Rhesus macaque mother-infant dyads (Macaca mulatta-N = 176) were observed twice weekly, with each session lasting 300 s. First-generation mothers were raised in one of three conditions: as mother-reared controls (MR; [n = 95]), in peer groups (PR; raised without adults but with constant access to three same-aged peers [n = 49]), or with an inanimate surrogate (SPR; raised with an inanimate fleece-covered, surrogate mother and limited daily peer-group interactions [n = 32]). Second-generation infants were all raised by their differentially reared mothers and statistically grouped into one of two groups: those that were rejected by their mothers beginning at a more-typical weaning age (controls), starting in the third month of life (n = 108), and those that were prematurely rejected, with mothers showing rejections before the third month of infant life (n = 68). Overall, PR mothers exhibited the highest rates of premature infant rejection, except for month 1 of infant life, when SPR mothers exhibited the highest rates of rejection. Intriguingly, after month 1, SPR mothers showed high rates of infant cradling and seldom rejected their infants. Independent of their mothers' early rearing environment, prematurely rejected infants displayed more aggression and passive vigilance, and were cradled and groomed less by their mothers, and there was evidence that the overall rates of rejection after the first 2 months of life had a cumulative negative effect on the developing infant. Post hoc analyses of plasma cortisol levels showed that the prematurely rejected infants had higher cortisol concentrations, suggesting a high level of stress in the prematurely rejected infants. These results suggest that maternal presence during infancy has long-term effects on a female's future maternal skills which, in turn, have intergenerational consequences for the socioemotional development of second-generation infants.

Rank acquisition is a developmental milestone for young primates, but the processes by which primate yearlings attain social rank in the absence of the mother remain unclear. We studied 18 maternally reared yearling rhesus macaques (Macaca mulatta) that differed in their social and physical rearing environments. We found that early social experience and maternal rank, but not individual traits (weight, sex, age), predicted dominance acquisition in the new peer-only social group. Yearlings also used coalitions to reinforce the hierarchy, and social affiliation (play and grooming) was likely a product, rather than a determinant, of rank acquisition. Following relocation to a familiar environment, significant rank changes occurred indicating that familiarity with a physical environment was salient in rank acquisition. Our results add to the growing body of literature emphasizing the role of the social and physical environment on behavioral development, namely social asymmetries among peers.

Though cognitive testing of infant monkeys has been practiced for the past 40 years, these assessments have been limited primarily to nursery-reared infants due to the confounds of separating mother-reared infants for assessments. Here, we describe a pilot study in which we developed a cognitive testing apparatus for socially housed, mother-peer-reared rhesus macaques under 1 year of age (Macaca mulatta) that allowed the infants to freely return to their mothers for contact comfort. Infants aged 151.2 ± 18.3 days (mean ± SEM; n = 5) were trained and tested on an object detour reach task. Infants completed training in 5.0 ± 0.2 days, and completed testing in 6.2 ± 0.9 days. Across 4 days of testing, infants improved to nearly errorless performance (Friedman test: χ(2) = 13.27, df = 3, p = 0.004) and learned to do the task more quickly (Friedman test: χ(2) = 11.69, df = 3, p = 0.009). These are the first cognitive data in group-housed, mother-peer-reared rhesus monkeys under 1 year of age, and they underscore the utility of this apparatus for studying cognitive development in a normative population of infant monkeys.

Previous studies suggest that about 50% of rhesus macaque infants engage in neonatal imitation of facial gestures. Here we measured whether individual differences in newborn macaques' (n = 49) visual attention may explain why some infants imitate lipsmacking (LPS) and tongue protrusion (TP) gestures. LPS imitators, but not TP imitators, looked more to a human experimenter's face and to a control stimulus compared to nonimitators (p = .017). LPS imitation was equally accurate when infants were looking at faces and when they were looking away (p = .221); TP imitation was more accurate when infants were looking at faces (p = .001). Potentially, less attention is necessary for LPS imitation compared to TP imitation, as LPS is part of macaques' natural communicative repertoire. These findings suggest that facial gestures may differentially engage imitators and nonimitators, and infants' visual attention during neonatal assessments may uncover the conditions that support this skill.

Kinematic studies of reaching in human infants using two-dimensional (2-D) and three-dimensional (3-D) recordings have complemented behavioral studies of infant handedness by providing additional evidence of early right asymmetries. Right hand reaches have been reported to be straighter and smoother than left hand reaches during the first year. Although reaching has been a popular measure of handedness in primates, there has been no systematic comparison of left and right hand reach kinematics. We investigated reaching in infant rhesus monkeys using the 2-D motion analysis software MaxTRAQ Lite+ (Innovision Systems). Linear mixed-effects models revealed that left hand reaches were smoother, but not straighter, than right hand reaches. An early left bias matches previous findings of a left hand preference for reaching in adult rhesus monkeys. Additional work using this kind of kinematic approach will extend our understanding of primate handedness beyond traditional studies measuring only frequency or bouts of hand use.

We examined the effects of early rearing experience on the development of dominance status in 53 juvenile (age 3) and then in 38 adult (ages 5-8) rhesus macaques. Based on previous research investigating the behavioral outcomes of nursery-rearing, we predicted that mother-reared (MR) monkeys would outrank peer-only reared (PR) monkeys, which would in turn outrank surrogate/peer-reared (SPR) subjects. Juvenile MR and PR subjects did not differ in ranks, but monkeys from both rearing backgrounds outranked SPR cage-mates at age 3. Independent of rearing condition, high-ranking juveniles gained the most weight between ages 1-3, suggesting that low status may be associated with decreases in early weight gain. Adult MR subjects outranked both PR and SPR subjects, with PR animals occupying intermediate ranks. These results indicate that impoverished early experiences, such as adult absence and limited social interaction, are useful predictors of future social success in rhesus macaques.

Though cognitive testing of infant monkeys has been practiced for the past 40 years, these assessments have been limited primarily to nursery-reared infants due to the confounds of separating mother-reared infants for assessments. Here, we describe a pilot study in which we developed a cognitive testing apparatus for socially housed, mother-peer-reared rhesus macaques under 1 year of age (Macaca mulatta) that allowed the infants to freely return to their mothers for contact comfort. Infants aged 151.2 ± 18.3 days (mean ± SEM; n = 5) were trained and tested on an object detour reach task. Infants completed training in 5.0 ± 0.2 days, and completed testing in 6.2 ± 0.9 days. Across 4 days of testing, infants improved to nearly errorless performance (Friedman test: χ(2) = 13.27, df = 3, p = 0.004) and learned to do the task more quickly (Friedman test: χ(2) = 11.69, df = 3, p = 0.009). These are the first cognitive data in group-housed, mother-peer-reared rhesus monkeys under 1 year of age, and they underscore the utility of this apparatus for studying cognitive development in a normative population of infant monkeys.

In this research we examined stress-related correlates of hand preference in monkeys. Specifically, we tested the hypothesis that stress reactivity and plasma levels of the stress hormone cortisol are developmentally related to handedness in rhesus macaques (Macaca mulatta). We found a significant positive correlation between cortisol levels sampled in juveniles and the frequency of right- versus left-hand use sampled in these same animals during adulthood. Right-hand preference was negatively correlated with stress reactivity. These data are consistent with the view that stress functioning and reactivity are associated with the development of hemispheric specialization in primates.

In this research we examined the relationship between plasma cortisol and handedness in infant rhesus macaques (Macaca mulatta). Specifically, we tested the hypothesis that stress functioning is related to hemispheric specialization and manifested in a positive correlation between cortisol levels and the frequency of right- versus left- hand use. We found a significant positive relationship between cortisol levels sampled at ages 1 and 3 months and lateral bias toward greater use of the right hand versus left hand sampled between ages 4 and 11 months. Further, we found a significant negative relationship between cortisol sampled at age 5 months and strength of lateral bias (independent of direction). These data suggest an early developmental influence of stress functioning on hemispheric specialization for manual control in infant monkeys.

In this research, we examined the relationship between handedness and levels of plasma cortisol in infant monkeys (Cebus apella). Specifically, we sought to test the hypothesis that stress functioning is related to hemispheric specialization and is manifested in a positive correlation between cortisol levels and the frequency of right- versus left-hand use. We found a significant relationship between stress cortisol at age 6 months and lateral bias towards greater use of the right versus left hand at ages 6 and 12 months. These data suggest an early developmental influence of stress reactivity on the emergence of hemispheric specialization for manual control in infant monkeys through the 1st year of postnatal life. © 2000 John Wiley & Sons, Inc. Dev Psychobiol 36: 213–217, 2000

We investigated the development of lateral bias in infant tufted capuchins (Cebus apella) by recording head orientation during the first 2 postnatal weeks and hand preference during Weeks 23 to 24 and 47 to 48. We found that lateral bias for head orientation at 1 to 2 weeks was negatively related to hand preference at 23 to 24 weeks. Further, we found population-level left-hand preferences at both 23 to 24 and 47 to 48 weeks, and that hand preference at 23 to 24 weeks is positively correlated with hand preference at 47 to 48 weeks. We also noted a trend toward a sex difference in the direction of neonatal head orientation, with males exhibiting a left-side preference and females exhibiting a lack of preference toward either side. Our findings differ from those obtained in studies with developing humans and chimpanzees in two important ways. First, the trend for head orientation and hand preference in infant capuchins was to the left rather than to the right. Second, we found a negative relation between direction of early head orientation and subsequent hand preference. It seems likely that research examining cerebral development in capuchins will help us to better understand the occurrence of left-handedness and the development of cerebral dominance in humans. © 1998 John Wiley & Sons, Inc. Dev Psychobiol 32: 45–50, 1998

We examined lateral bias for looking, reaching, and turning in 33 tufted capuchin monkeys (Cebus apella) comprising 29 parent–offspring dyads (13 mother–offspring dyads and 16 father–offspring dyads). We found evidence for maternal and paternal contributions to the direction of looking bias but no evidence for contribution from either parent to the direction of reaching bias. Further, we found evidence of differential maternal and paternal influences on the direction of offspring turning bias. Finally, we found no evidence of parental contribution to the strength of lateral bias for any of our measures. Our results indicate that parental contributions to lateral bias in humans and apes may not correspond to those in monkeys. ©1997 John Wiley & Sons, Inc. Dev Psychobiol 31: 143–147, 1997

Strain differences in temperament and physiology have been reported for several animal species, but nonhuman primates have not been well studied in this regard. We assessed behavior and physiology in Chinese–Indian hybrid (n = 13) and Indian-origin (n = 29) nursery-reared rhesus monkey infants. Previous data indicate that Chinese-origin and Chinese–Indian hybrid rhesus exhibit more aggression directed toward humans and conspecifics and are more irritable in response to neonatal assessment procedures than are Indian-derived rhesus. In addition, in rhesus adults, low levels of cerebrospinal fluid 5-HIAA have been correlated with impulsivity, aggressive behavior, and diminished social competence. We therefore hypothesized that hybrid infants would exhibit more behavioral and adrenocortical reactivity in the home cage and during social separations, would be less sociable in their peer groups, and would exhibit lower CSF 5-HIAA levels than Indian-derived monkeys. Blood and cerebrospinal fluid samples were obtained on Days 14, 30, 60, 90, 120, and 150 of life, and prior to and during social separations at 6 months of age. Behavioral observations were conducted in the home cage and during the separation condition. No differences in behavior were observed between hybrid and Indian-derived animals in the home cage. Indian-derived and hybrid infants exhibited diverging patterns of behavioral reactivity across the 4 weeks of the repetitive social-separation procedure, and during reunion periods. Although plasma cortisol levels were sensitive to the testing conditions, no group differences were observed. CSF 5-HIAA declined over time for all monkeys, and hybrid animals exhibited significantly lower 5-HIAA levels than Indian monkeys beginning at 6 months of age. These findings are consistent with the known behavioral and physiological characteristics of Chinese-origin adult rhesus. ©1997 John Wiley & Sons, Inc. Dev Psychobiol 31: 49–63, 1997

Adverse early experiences are associated with a range of deleterious health outcomes in humans, including higher risk for affective disorders. Studies using a long-standing model of nonhuman primate model of early adversity have demonstrated that nursery-reared monkeys exhibit alterations in multiple aspects of biobehavioral development; however, few studies have evaluated the persistence of socioaffective behavioral changes through adulthood. We evaluated the effects of early rearing experience on adult animals’ response to a well-validated assessment of anxiety-like behavior, the Human Intruder Paradigm (HIP). We tested twenty-two rhesus monkeys who were either nursery-reared (NR) or reared with their mothers (mother-reared; MR). NR monkeys were inhibited in their behavior compared to MR monkeys, with reduced locomotion and exploratory behaviors. NR animals showed a marginal increase in freezing. Together these findings demonstrate that the consequences of differential infant rearing experience on socioaffective behavior persist into adulthood, with evidence of greater inhibition in NR monkeys.

Levels of tetanus-specific antibodies were assessed in free-ranging, yearling rhesus monkeys following prophylactic immunization with tetanus toxoid. Each subject's behavior had been observed between 11 and 25 weeks of age and approximately 2 months later during its mother's first concentrated mating period as a part of another study. Prior to immunization, at approximately 1 year of age, cardiovascular parameters, and several plasma parameters [cortisol, adrenocorticotrophic hormone (ACTH), growth hormone (GH), interleukin-2 (IL-2), and total plasma immunoglobulin G (IgG)] were measured during a brief period of captivity. Antibody titers noted approximately 2 weeks after immunization were related to cardiovascular parameters. Thus, yearlings with high heart rates and low heart rate variability during captivity had the highest tetanus-specific serum IgG. Levels of plasma cortisol, ACTH, total IgG, and IL-2 noted at the time of capture were unrelated to subsequent antibody levels. Antibody titers were, however, positively correlated with GH noted immediately following capture on the day prior to immunization. Antibody titers were also related to the infants' behavior observed during their mother's first concentrated mating period, Infants who were most distressed (high levels of distress vocalization) when their mother resumed mating (a time particularly stressful for free-ranging rhesus infants) showed lower antibody titers to tetanus immunization as a yearling. The present observations add support to the existence of a relationship between behavior during exposure to an early stressor and later immune regulation and that certain cardiovascular parameters may be related to certain indicators of immunoregulation. © 1993 John Wiley & Sons, Inc.

Recent studies have revealed that human infants process female faces differently from male faces. To test whether a similar preference for female faces exists in other primates, we presented nursery-reared infant rhesus macaques with photographs of macaque faces and human faces. At less than 1 month old, infant macaques preferentially oriented towards female macaque faces when faces were presented upright. No preference for female human faces was found. At 9 months old, infants failed to show a visual preference for female macaque faces or female human faces, although they showed significantly more lipsmacking responses at female human faces. Compared to human infants, macaques appear to have stronger predispositions early in life but this preference may nonetheless be amendable to experience. Understanding how innate predispositions and the social rearing environment shape infants’ understanding of faces remain important issues to be explored in order to understand facial processing abilities in humans and other primates.

Although high circulating levels of glucocorticoids are associated with impaired cognitive performance in adults, less is known about this relationship in infancy. Furthermore, because studies have relied on acute cortisol measures in blood plasma or saliva, interpretation of the results may be difficult as acute measures may in part reflect emotional responses to testing procedures. In this study we examined whether hair cortisol, an integrated measure of hypothalamic–pituitary–adrenal (HPA) axis functioning, predicted performance of nursery-reared (NR) infant rhesus monkeys (n = 32) on Piagetian object permanence tasks. Testing of NR infants began at 19.8 ± 2.2 (mean ± SE) days of age and continued for the next several months. Hair cortisol concentrations from the 32 NR monkeys were compared to those of 20 mother–peer-reared (MPR) infants. Hair was shaved at Day 14, allowed to regrow, and obtained again at month 6, thus representing integrated cortisol over a 5.5-month period of time. NR and MPR infants did not differ in month 6 hair cortisol values (t(50) = 0.02, p = 0.98). Linear regression revealed that hair cortisol predicted object permanence performance in the NR infants. Infants with higher hair cortisol reached criterion at later ages on the well (p

This study investigated relationships between withdrawal behaviors in rhesus macaques and changes in monoamine metabolite and endocrine concentrations during repeated psychosocial stress. Rhesus monkeys (N = 71) experienced maternal separation in which four separations took place during four consecutive weeks. Behavioral observations were made, as well as plasma concentrations of cortisol and cerebrospinal fluid concentrations of the serotonin, dopamine, and norepinephrine metabolites were obtained. Animals were assigned to high, moderate, and low withdrawal groups, defined using baseline durations of withdrawal behaviors. Highly withdrawn animals showed less reduction than nonwithdrawn animals in serotonin metabolite concentrations over repeated separations. Highly withdrawn macaques also failed to significantly reduce cortisol concentrations across separation weeks. More adaptation in central serotonin functioning and cortisol concentrations was seen in nonwithdrawn primates than in highly withdrawn primates; these findings have implications for increased risk of developing anxiety disorders in highly inhibited children.

While developmental researchers have long noted that infants of many mammalian species, including primates, have characteristic physical features, such as a distinctive coat or skin color, and some authors have further suggested that these features serve to elicit caretaking and solicitous behavior, few systematic investigations of the actual salience of such features for adult conspecifics have been carried out to date. The present series of 3 studies sought to determine whether natal coat and/or facial skin coloration might provide desirable visual stimulation for rhesus monkey adult females. In these studies the faces and/or fur of 6-month-old rhesus monkeys were dyed to simulate the normal coloration of rhesus monkey neonates. Adult females varying in parity and rearing history were then tested for their relative preference between these infantile-colored 6-month-olds and both normally colored 6-month-olds and other differentially colored control stimulus monkeys. Results indicated that regardless of parity or rearing history the adult female subjects exhibited consistent preferences for the stimulus animals with neonatal-like reddish-pink facial skin coloration.