A periodic dosing model of fetal alcohol syndrome in the pig-tailed macaque (Macaca nemestrina)

A nonhuman primate on a periodic ethanol dosing schedule should provide a model of fetal alcohol syndrome (FAS) most relevant to the majority of pregnant women who are “social drinkers” and can exercise reasonable control over their ethanol intake. In this pilot study, four pregnant pig-tailed macaques (Macaca nemestrina) received ethanol once a week from 40 days' gestation. Doses were 2.5 gm/kg for three moderate-dose animals (MDAs) and 4.1 gm/kg for one high-dose animal (HDA). Peak blood ethanol levels reached a mean of 240–256 mg/dl for the MDAs and averaged 379 mg/dl for the HDA. Peak acetaldehyde did not vary with dose. One MDA aborted after the first dose. The other three pregnancies were compared with eight to ten control pregnancies, and the infants' development over the first six months was compared with that of the control offspring. Nutritional status of the pregnant females was normal. The fetal heart rate response to maternal restraint was absent in the HDA. Gestational duration and simian Apgar scores were normal. All three infants were abnormally large, and two were also abnormally heavy, with body weight appropriate to skeletal size. Skeletal maturation, judged by ossification and tooth eruption, was not accelerated. The high-dose infant (HDI) was scaphocephalic, with an underdeveloped cranial base and midface, and its brain was small and dysplastic; its reflex, motor, and cognitive development were retarded. One moderate-dose infant (MDI) had some brain abnormalities; it was hyperkinetic and showed developmental retardation on several behavioral measures. The other MDI was normal. We conclude that the periodic model offers an effective means of investigating FAS in M. nemestrina. Furthermore, when nutrition is maintained, intermittent intake of ethanol by the pregnant primate does not necessarily reatard fetal growth.     

What defines successful integration into a social group for hand-reared chimpanzee infants?

Hand-rearing of captive great ape infants is sometimes necessary but can have negative behavioral consequences. Modern hand-rearing protocols, including early integration into a diverse group of conspecifics, appear to reduce the negative consequences of hand-rearing, but the process of integration is not well studied. We investigated six potential metrics of success during the introduction of two hand-reared chimpanzee infants into a troop of nine other chimpanzees at the Maryland Zoo in Baltimore. Little aggression was observed and the infants continue to be maintained in the troop at publication. As we predicted, during the introduction the hand-reared infants showed consistent levels of stress-related behaviors, participated in affiliative interactions with all available partners, and acted, received, and mutually engaged in these interactions. Solitary behaviors by these infants were similar to a mother-reared infant in the same group. Each infant also formed a relationship with a specific female that involved nest-sharing, carrying, retrieval, and intervening to reduce risk to the infant; these relationships could be classified as allomothering because they involved maternal behavior but occupied significantly less of the infants’ time than a maternal relationship. Contrary to our prediction, the hand-reared infants therefore spent significantly less time in social behavior than a mother-reared infant of the same age. In addition, the hand-reared infants continued to show strong social preferences for each other as introductions progressed and to direct a low but consistent number of nonfeeding social behaviors to humans. The successful introduction of hand-reared infants appeared to involve adding conspecific social relationships to the infants’ social repertoire, but not eliminating social interactions directed at humans.     

Temperament in Rhesus,Long‐Tailed,and Pigtailed Macaques Varies by Species and Sex

Temperament differs among individuals both within and between species. Evidence suggests that differences in temperament of group members may parallel differences in social behavior among groups or between species. Here, we compared temperament between three closely related species of monkey—rhesus (Macaca mulatta), long‐tailed (M. fascicularis), and pigtailed (M. nemestrina) macaques—using cage‐front behavioral observations of individually housed monkeys at a National Primate Research Center. Frequencies of 12 behaviors in 899 subjects were analyzed using a principal components analysis to identify temperament components. The analysis identified four components, which we interpreted as Sociability toward humans, Cautiousness, Aggressiveness, and Fearfulness. Species and sexes differed in their average scores on these components, even after controlling for differences in age and early‐life experiences. Our results suggest that rhesus macaques are especially aggressive and unsociable toward humans, long‐tailed macaques are more cautious and fearful, and pigtailed macaques are more sociable toward humans and less aggressive than the other species. Pigtailed males were notably more sociable than any other group. The differences observed are consistent with reported variation in these species’ social behaviors, as rhesus macaques generally engage in more social aggression and pigtailed macaques engage in more male–male affiliative behaviors. Differences in predation risks are among the socioecological factors that might make these species‐typical behaviors adaptive. Our results suggest that adaptive species‐level social differences may be encoded in individual‐level temperaments, which are manifested even outside of a social context. Am. J. Primatol. 75:303‐313, 2013. © 2012 Wiley Periodicals, Inc.     

Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

Relationship of early infant state measures to behavior over the first year of life in the tufted capuchin monkey (Cebus apella)

Data on activity states were collected from 29 group-housed capuchin monkey (Cebus apella) infants for 3 h each week from birth to 11 weeks of age. The amounts of time spent in sleeping/drowsy, alert–quiet, and alert–active states were measured in these subjects. Videotaped observations of these infants were recorded 3 times/week in the home cage over the first year of life and were scored for a number of social and exploratory behaviors. The extent to which early infant activity state scores predicted later behavior in the home cage was examined. Infant state measures correlated significantly with home cage behavior during months 2–6 in that infants that had been more active in early infancy spent more time alone, with other animals, and in exploration and play and less time with mothers than did quieter infants. Early state measures were less successful in predicting home cage scores beyond 8 months of age, whereas differences in behavior attributable to housing variables became more salient in the latter part of the first year. There was also a negative correlation between mother and infant activity in months 2 and 3, in that more sedentary mothers tended to have more active infants. Am. J. Primatol. 44:43–56, 1998. © 1998 Wiley-Liss, Inc. This article is a U.S. Government work, and, as such, is in the public domain in the United States of America.     

Lactational programming? mother's milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta)

There are many aspects of “mothering” that may provide information to the mammalian infant about environmental conditions during critical periods of development. One essential element of mothering involves the quantity and quality of milk that mothers provide for their infants, but little is known about the consequences of variation in milk production. Mother's milk may affect infant behavior by contributing to brain development and to the development of behavioral dispositions. Here we present the first evidence for any mammal that natural variation in available milk energy (AME) from the mother is associated with later variation in infant behavior and temperament in rhesus macaques (Macaca mulatta, N=59). In the early postnatal period, heavier mothers with more reproductive experience produced greater AME, which is the product of milk energy density (kcal/g) and milk yield (g). Moreover, infants whose mothers produced greater AME in the early postnatal period showed higher activity levels and greater confidence in a stressful setting later in infancy. Our results suggest that the milk energy available soon after birth may be a nutritional cue that calibrates the infant's behavior to environmental or maternal conditions. These data provide new insight into potential mechanisms for the development of behavior and temperament and illuminate new directions for investigating maternal effects, nutritional programming, and developmental plasticity. Am. J. Primatol. 72:522–529, 2010. © 2010 Wiley‐Liss, Inc.     

Pair-rearing infant monkeys (Macaca nemestrina) using a “rotating-peer” strategy

Appropriate rearing conditions for captive primates are important for both research and breeding purposes. In an earlier study, pigtailed macaque infants that were pair-reared with a single continuous partner exhibited excessive social clinging and could not adapt to living in large social groups at 8–10 months of age. In the present study, eight macaques were pair-reared until they were 6 months old. Each member of an animal's four-monkey social group served as a home-cage partner. In an attempt to reduce excessive mutual clinging, the pairs were rotated every 2–3 days to increase the variability of social stimulation in the home cage. However, these infants developed abnormal social behaviors that were in some cases even more extreme than those exhibited by infants pair-reared with a single continuous partner. A second goal of this experiment was to study interlaboratory reliability for the development of social behavior. The animals were divided into two groups, one housed in a nursery and the other in a biological safety level 3 virus laboratory. Some differences were detected between the two groups, demonstrating the necessity of controls in biobehavioral developmental research. Am. J. Primatol. 41:141–149, 1997. © 1997 Wiley-Liss, Inc.     

Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infant rhesus macaques (Macaca mulatta)

In several primate species, males have been shown to exhibit a surge in circulating testosterone during the early postnatal period. This surge has been postulated to play a role in the development of sex differences in behavior. In this study, the role of postnatal testosterone in infant behavioral development was investigated in socially living rhesus macaques. Seven male infants were treated with a GnRH agonist, avorelin, from the first week of life onwards. Ten female infants were exposed to testosterone by implantation of capsules containing testosterone. The behavioral development of these and control infants was recorded from birth to 6 months of age. The sexually dimorphic patterns of play and mounting were not affected by manipulation of postnatal testosterone in either male or female infants. Similarly, most mother-infant interactions were not affected by the hormonal manipulation of infants. Mothers of testosterone-treated females were found to take more responsibility for moving into and out of arm's reach of their infants than mothers of some other groups of infants; however, this measure did not normally differ between mothers of male and female infants. Manipulation of the postnatal testosterone surge does significantly affect penile growth and development, but does not affect the expression of infant sex differences in behavior nor greatly affect the development of the mother-infant relationship in rhesus macaques.     

Maternal caregiving and DNA methylation in human infants and children: Systematic review

The integration of behavioral epigenetics' principles (eg, DNA methylation) into the study of human infants' development has mainly focused on the effects of early adverse exposures, paying less attention to protective caregiving experiences. The present review focused on DNA methylation linked to variations in maternal behavior in human infants and children. Literature search occurred on three databases (PubMed, Scopus and Web of Science) and 11 records were selected. Key variables were abstracted from each article including: sample size and characteristics, time and type of maternal caregiving behavior exposure, time and locus of methylation biomarker, presence/absence, time and type of adverse exposure. Six out of eleven records documented the predictive effect of maternal caregiving on DNA methylation, whereas the remaining five reported on the role of maternal behavior as an influencing factor of the adversity‐to‐methylation link. Consistent with evidence from the animal model, the quality of maternal caregiving in humans (a) might be associated with variations in DNA methylation status of specific genes involved in socio‐emotional development and (b) might partially buffer the association between early adversities and epigenetic variations in infants and children. Current evidence suggests that the quality of maternal caregiving can contribute to behavioral development trajectories of human infants and children at least partially through epigenetic regulation. Open questions and methodological aspects are discussed to guide future human developmental research in behavioral epigenetics.     

An experimental study of vocal communication between mother and infant monkeys (Macaca nemestrina)

Vocal communication was studied in six feral-born mother monkeys (Macaca nemestrina) and their three- to four-month-old infants in tests which employed two sound-shielded rooms equipped with microphones and speakers. The mothers' locomotor activity levels were measured as activity counts, and vocalizations of mothers and infants were recorded under three conditions: mothers in two-way auditory communication with their own infants, in two-way auditory communication with other infants of matched sex and age, and without communication. Mothers' vocalizations and activity counts during auditory access were correlated with the number of infants' vocalizations in the same tests. Mothers' activity counts were higher with auditory access to an infant. However, neither activity counts nor vocalizations of mothers differed when in communication with their own infants from the same measures when in communication with matched infants. Neither mothers nor infants vocalized differently, either qualitatively or quantitatively, in the three conditions.     

Growth and development of the term and premature pig-tailed macaque (Macaca nemestrina): Cardiovascular and respiratory changes during the first 3 weeks of life

Growth and development of the infant pigtailed macaque (Macaca nemestrina) over the first 3 weeks of life have been characterized by the variables of body weight, blood pressure, heart rate, ventilation, blood gas tensions, and lung mechanics. The effects of prematurity on postnatal developmental trends were assessed at gestational ages of 135–145 days (0.80 of term) and 150–155 days (0.91 of term). There was no indication that cesarean section, restraint, or instrumentation had any significant influence on the measurements. Gestational age at delivery had no effect on the minute ventilation per kilogram body weight, the hematocrit, or the heart rate; however, body weight, tidal volume, respiratory frequency, arterial gas tensions, blood pressure, and lung compliance did vary with gestational age at delivery. Postnatal maturational changes in these variables were similar between term and premature animals. The data for infant macaques and newborn humans were compared. The newborn macaque appears to be an excellent model of human developmental trends (and/or disease state) over the first 3 weeks of life, though some potentially important differences have been found.     

Birth Timing and Behavioral Responsiveness Predict Individual Differences in the Mother–Infant Relationship and Infant Behavior During Weaning and Maternal Breeding

There is a great deal of variability in mother–infant interactions and infant behavior across the first year of life in rhesus monkeys. The current article has two specific aims: (1) to determine if birth timing predicts variability in the mother–infant relationship and infant behavior during weaning and maternal breeding, and (2) to identify predictors of infant behavior during a period of acute challenge, maternal breeding. Forty‐one mother–infant pairs were observed during weaning when infants were 4.5 months old, and 33 were followed through maternal breeding. Subjective ratings of 16 adjectives reflecting qualities of maternal attitude, mother–infant interactions, and infant attitude were factor analyzed to construct factors relating to the mother–infant relationship (Relaxed and Aggressive) and infant behavior (Positive Engagement and Distress). During weaning, late born infants were more Positively Engaged than peak born infants (ANOVA, P < 0.05); however, birth timing did not affect the mother–infant relationship factors Relaxed and Aggressive or the infant attitude factor Distress. During maternal breeding, early born infants had less Relaxed relationships with their mothers than peak or late born infants, higher Positive Engagement scores than peak or late born infants, and tended to have higher Distress scores than peak born infants (repeated‐measures ANOVA, P < 0.05). In addition, Distress scores were higher during maternal breeding than during the pre‐ and postbreeding phases. Finally, multiple regression (P < 0.05) indicated that while infant behavioral responsiveness predicted infant Positive Engagement during the acute challenge of maternal breeding, qualities of the mother–infant relationship predicted infant Distress. These data suggest that birth timing influences the patterns of mother–infant interactions during weaning and maternal breeding. Additionally, infant behavioral responsiveness and mother–infant relationship quality impact infant social engagement and affect expression, respectively. Am. J. Primatol. 74:734‐746, 2012. © 2012 Wiley Periodicals, Inc.     

Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch)

The purpose of this study was to describe patterns of infant care and development in family groups of the monogamous titi (Callicebus moloch). Three infant titis were observed with their natal family groups over the first six months of life. Field observations of extensive male involvement with infants were confirmed. Adult males were clearly the infants' primary social companions, and infants spent more time in contact with adult males at all ages than with mothers or older siblings. However, mothers and siblings also carried infants at times and interacted with them in affiliative ways (e.g., grooming, nuzzling, play). Mothers often invited nursing, but otherwise it was infants who primarily initiated transfers between carriers and approaches to parents, reminding us that the infants' own activities and their effects on caregivers should not be overlooked in considerations of the patterns of infant care. This is particularly important for those species exhibiting extensive parental involvement by males. It is suggested that substantial male care of young titi infants leads to several important consequences for the infant's social development, including the development of a stronger attachment to the father than the mother.     

Early social environment interferes with the development of NADPH–diaphorase‐reactive neurons in the rodent orbital prefrontal cortex

The influence of early parental deprivation on the development of NADPH–diaphorase–(NO‐synthase) reactive neuron numbers in subregions of the orbital prefrontal cortex (ventrolateral orbital, lateral orbital, and agranular insular cortex) was quantitatively investigated in the precocious lagomorph Octodon degus. Forty‐five‐day‐old degus from three groups were compared: (1) repeated parental separation: degus that were repeatedly separated from their parents during the first three postnatal weeks and thereafter raised in undisturbed social conditions; (2) chronic isolation: degus that were raised under undisturbed social conditions until postnatal day 21, and then were reared in chronic social isolation; and (3) control: degus that were reared undisturbed in their families. Compared to the control animals the ventrolateral orbital prefrontal cortex and agranular insular cortex of the two deprived groups displayed significantly decreased density of NADPH–diaphorase‐reactive neurons (down to 62% in the ventrolateral orbital prefrontal cortex of males, 70% in the agranular insular cortex, and in the lateral orbital prefrontal cortex 80% in both genders). These results confirm that early changes of social environment interferes with the development of limbic circuits, which might determine normal or pathological behaviors in later life. © 2004 Wiley Periodicals, Inc. J Neurobiol, 2005     

Sex differences in use of a species-typical facial gesture by pigtail monkeys (Macaca nemestrina)

A species-typical gesture, the “jaw thrust”, was sequentially analyzed in a group of adultM. nemestrina. The major finding was a sex difference in apparent function with male jaw thrust sequences most likely to result in sexual behavior and female sequences most likely to terminate in agonistic behavior. Sex differences in the initiation and reception of jaw thrusts were also observed; they were most commonly initiated by males and directed toward females. Marked stereotypy of the behavioral sequences including jaw thrusts was observed: only a small proportion of the species’ behavioral repertoire was exhibited in temporal association with the gesture. Despite the striking nature of the gesture and the frequency with which it was exhibited, a majority of the signals had no overt social effect.     

Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8–10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.     

Early‐Life Exposure to Pulsed LTE Radiofrequency Fields Causes Persistent Changes in Activity and Behavior in C57BL/6 J Mice

Despite much research, gaps remain in knowledge about the potential health effects of exposure to radiofrequency (RF) fields. This study investigated the effects of early‐life exposure to pulsed long term evolution (LTE) 1,846 MHz downlink signals on innate mouse behavior. Animals were exposed for 30 min/day, 5 days/week at a whole‐body average specific energy absorption rate (SAR) of 0.5 or 1 W/kg from late pregnancy (gestation day 13.5) to weaning (postnatal day 21). A behavioral tracking system measured locomotor, drinking, and feeding behavior in the home cage from 12 to 28 weeks of age. The exposure caused significant effects on both appetitive behaviors and activity of offspring that depended on the SAR. Compared with sham‐exposed controls, exposure at 0.5 W/kg significantly decreased drinking frequency (P ≤ 0.000) and significantly decreased distance moved (P ≤ 0.001). In contrast, exposure at 1 W/kg significantly increased drinking frequency (P ≤ 0.001) and significantly increased moving duration (P ≤ 0.005). In the absence of other plausible explanations, it is concluded that repeated exposure to low‐level RF fields in early life may have a persistent and long‐term effect on adult behavior. Bioelectromagnetics. 2019;40:498–511. © 2019 The Authors. Bioelectromagnetics Published by Wiley Periodicals, Inc.     

Serotonin transporter expression is predicted by early life stress and is associated with disinhibited behavior in infant rhesus macaques

Serotonin transporter (5-HTT) expression patterns may contribute to the risk for adverse psychological outcomes following early life stress. The present study investigated whether two types of early life stress, maternal and social aggression, and a serotonin transporter gene promoter polymorphism ( rh5-HTTLPR ) predicted lower post-stressor peripheral blood mononuclear cell (PBMC) 5-HTT expression in infant rhesus macaques. We further probed the relationships among these factors and infant behavioral disinhibition within a stressful situation. Fifty-three infants residing with mothers in large, complex social groups were observed over the first 12 postnatal weeks, during which time the rate of aggression received by the infant from their mothers and social group members was recorded. At 90–120 days of age, infants underwent a 25-h maternal separation/biobehavioral assessment, which included standardized behavioral assessments and blood sampling. Infants' rh5-HTTLPR genotypes were determined, and infant 5-HTT expression was quantified from PBMCs collected 8 h after separation. Receipt of aggression from the mother, but not from social group members, was associated with lower post-stressor 5-HTT expression. Lower post-stressor 5-HTT expression, but not receipt of aggression, was associated with disinhibited behavior during assessment. Rh5-HTTLPR genotype was unrelated to any measure. We conclude that 5-HTT regulation is linked with specific, presumably stressful early experiences in infant rhesus macaques. Further, 5-HTT expression predicted behavioral disinhibition, presumably via parallel processes that operate in the brain.     

Development of children adopted to the United States following a social–emotional intervention in St. Petersburg (Russian Federation) institutions

This study is a post-adoption follow-up of social–emotional interventions in St. Petersburg, Russian Federation Baby Homes (BHs). Children previously resided in BHs and received Care as Usual (CAU, N?=?220), Training Only (TO, N?=?94), or Training plus Structural Changes (T?+?SC, N?=?45). This study examined intervention effects 0–6.5 years post-adoption to the United States, at age 9 months to 7 years old. Adoptive parents completed questionnaires on their child’s social and behavioral development. Intervention graduates had better attachment security, less indiscriminate friendliness, and fewer behavior problems than CAU graduates. Children who had longer exposure to intervention conditions had better attachment security, but poorer executive function, externalizing and internalizing problems, and competence. Thus, although postinstitutionalized children were generally functioning in the normal range in early childhood and effect sizes were small, a social–emotional intervention in institutions is associated with modest benefits to attachment and behavior problems and apparent decrements to executive function.