Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants.

A functional polymorphism in the promoter region of the serotonin transporter (5-HTTLPR) gene has been associated with variation in anxiety and hypothalamus-pituitary-adrenal (HPA) axis function in humans and rhesus macaques. Individuals carrying the short allele are at a higher risk for developmental psychopathology, and this risk is magnified in short allele carriers who have experienced early life stress. This study investigated the relationship between 5-HTTLPR allelic variation, infant abuse, and behavioral and hormonal responses to stress in rhesus macaques. Subjects were 10 abusive mothers and their infants, and 10 nonabusive mother-infant pairs. Mothers and infants were genotyped for the rh5-HTTLPR, and studied in the first 6 months of infant life. For mothers and infants, we measured social group behavior, behavioral responses to handling procedures, and plasma concentrations of ACTH and cortisol under basal conditions and in response to stress tests. The proportion of individuals carrying the short rh5-HTTLPR allele was significantly higher among abusive mothers than controls. Among mothers and infants, the short allele was associated with higher basal cortisol levels and greater hormonal stress responses in the infants. In addition, infants who carried the short rh5-HTTLPR allele had higher anxiety scores than infants homozygous for the long allele. The rh5-HTTLPR genotype also interacted with early adverse experience to impact HPA axis function in the infants. These results are consistent with those of previous studies which demonstrate associations between serotonergic activity and anxiety and stress reactivity, and add additional evidence suggesting that genetic variation in serotonergic function may contribute to the occurrence of abusive parenting in rhesus macaques and modulate emotional behavior and HPA axis function.

Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life.

We investigated the maternal care patterns of rhesus macaque mothers who physically abuse their infants, and compared their infants' behavior to that of nonabused infants. Parametric and multidimensional scaling analyses indicated that abusive mothers have a distinct parenting style characterized by high rates of rejection and contact-breaking from their infants. Compared to control infants, abused infants exhibited signs of delayed independence from their mothers including higher rates of distress calls and anxiety, lower rates of contact-breaking, and differences in play. Several aspects of the abused infants' behavior were correlated with rates of abuse received during the first month, or with other maternal behaviors. These findings provide a more comprehensive characterization of the parenting styles of abusive mothers and the early behavioral development of their infants than previously available. Detailed knowledge of the early experience of abused infants is crucial for understanding possible pathological alterations in behavior and neuroendocrine function later in life.

Measuring temperament in rhesus macaques: consistency and change in emotionality over time.

This study of rhesus macaques (Macaca mulatta) investigated whether individual differences in emotionality, as measured by scratching frequencies, are stable over time and across seasons. Five adult females living in captive social groups were observed during two consecutive birth seasons and five females during the birth and the mating season. Scratching frequencies were higher during the birth than during the mating season, suggesting that the presence of infants was associated with elevated emotionality. Individual differences in scratching frequencies remained stable across two consecutive birth seasons, but there was no significant correlation between scratching frequencies in the birth and in the mating season. These findings suggest that, under certain circumstances, individual differences in emotionality are consistent over time and that scratching may be used as a non-invasive indicator of temperament.

Crying and infant abuse in rhesus monkeys.

This study investigated the relation between crying and infant abuse in group-living rhesus monkeys (Macaca mulatta). The subjects were 10 abusive mothers with their infants and 10 control mother-infant pairs. Abused infants cried more frequently than controls in the first 12 weeks of life, even when cries immediately following abuse were excluded from the analysis. The coos of 5 abused infants differed from those of 5 controls in several acoustic parameters, whereas their screams and geckers were acoustically similar, when recorded in the same context. Abusive mothers were less likely than control mothers to respond positively to the cries of their infants. Although infant cries may increase the probability of abuse being repeated, infant crying per se does not appear to be a major determinant of abuse.

Behavioral and mesocorticolimbic dopamine responses to non aggressive social interactions depend on previous social experiences and on the opponent's sex.

In these experiments we evaluated the relationship between behavioral and brain dopamine (DA) responses to social interactions. Subjects were group housed male mice confronted with a non aggressive male or female conspecific following either repeated defeat (defeated) or repeated non aggressive experiences (social). Defeated mice showed more defensive/submissive reactions then mice of the social group regardless of the opponent sex. However, mice defeated by females showed reduced social exploration without significant differences in non social exploration whilst the opposite was true for mice defeated by male opponents. Non aggressive social interactions enhanced dopamine metabolism in the prefrontal cortex (pFC) of DEFEATED mice regardless of opponent sex. However, only mice defeated by females showed enhanced dopamine metabolism and release in the nucleus accumbens septi (NAS) and olfactory tubercle (OT) following interaction with the non aggressive opponent. Finally, correlation between central and behavioral responses evidenced that 3,4-dihydroxiphenilacetic acid levels in the pFC were positively correlated with defensive behaviors and negatively correlated with non social exploration in mice confronted with male opponents but not in those confronted with females. The latter, showed a significant positive correlation between 3-methoxytyramine (3-MT) levels in the OT and defensive responses and significant negative correlation between social investigation and 3-MT levels in the OT and in the NAS. These results indicate a strict relationship between mesocorticolimbic dopamine transmission and behavior responses to social cues. Moreover, they strongly support the view that mesocorticolimbic DA modulates social behavior by affecting perceptive processing.

Hormones and behavior in rhesus macaque abusive and nonabusive mothers. 2. Mother-infant interactions.

This study investigated the differences in parenting style and hormonal variables in abusive and nonabusive rhesus macaque mothers during the first 2 months of lactation. All subjects lived in large social groups in outdoor corrals. Abusive mothers were more protective and more rejecting of their infants than nonabusive mothers, particularly in the first month. Abusive and nonabusive mothers did not differ in levels of circulating estradiol (E2) and progesterone (P) during the periparturitional period except that the decrease in P after parturition was less marked in abusive than in nonabusive mothers. Individual differences in periparturitional E2 or P were not correlated with differences in parenting style. Mothers with higher frequencies of abuse, however, had significantly higher values of the E2-to-P ratio in the last week of pregnancy and significantly lower values of P in the first week of lactation than mothers with lower frequencies of abuse. Although pregnancy or lactation hormones are unlikely to be one of the main determinants of abusive behavior, endocrine variables may interact with personality characteristics or environmental factors in causing this phenomenon.

Hormones and behavior in rhesus macaque abusive and nonabusive mothers. 1. Social interactions during late pregnancy and early lactation.

This study investigated changes in hormone levels and social behavior during late pregnancy and early lactation in rhesus macaque abusive and nonabusive mothers. All subjects lived in large social groups in outdoor corrals. Estradiol and progesterone levels increased to a peak the week before parturition, dropped after parturition, and remained low thereafter. The hormonal profiles of abusive and nonabusive mothers were generally similar. There were few changes in social interactions involving contact, grooming, or aggression across pregnancy or lactation, and minor differences between abusive and nonabusive mothers. The transition to motherhood was accompanied by a reduction in active grooming and an increase in aggression, and such changes were more marked for abusive than nonabusive mothers. Some individual differences in social behavior were correlated with hormone levels during pregnancy, but not lactation. These findings suggest that although the endocrine changes underlying the periparturitional period may affect female social behavior, some of the social changes associated with motherhood are likely to reflect the presence of infants.

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.

Formal dominance: the emperor's new clothes?

I previously argued that formal dominance requires the ability to attribute knowledge to other individuals (D. Maestripieri, 1996). Formal dominance is otherwise indistinguishable from the way dominance has previously been conceptualized. For example, the notion that nonhuman primates have social relationships and that 2 individuals express their knowledge about the state of their relationship with signals of dominance and submission is intrinsic to the concept of dominance and not peculiar to formal dominance. Moreover, the claims made by formal dominance supporters that macaque signals such as the bared-teeth display are always displayed unidirectionally to other group members and never directed to predators are incorrect. If the mentalistic terms used to describe formal dominance must not be taken literally, then the interpretation of submissive signals such as the bared-teeth display from a formal dominance perspective remains unclear.

The biology of human parenting: insights from nonhuman primates.

Primate and human parenting have often been viewed as completely emancipated from neuroendocrine influences and primarily dependent on experience, social and cognitive processes. A review of recent findings of primate research on the neurobiological regulation of parental responsiveness, the causes of variability in parenting styles, and the determinants of infant abuse suggests that primate parenting is more sensitive to neuroendocrine mechanisms than previously thought. The findings of primate research can have important implications for human research and encourage the investigation of biological influences on human parenting.

Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants.

This study investigated the abusive behavior and parenting styles of 7 rhesus macaque mothers with infants born in 2 consecutive years. All subjects lived in captive social groups and were observed during the first 12 weeks of infant life. With the exception of 1 individual, mothers were generally consistent in the frequency with which they abused their successive infants. Similarities were also found in the temporal course of infant abuse, the use of the most common pattern of abuse, and some measures of parenting style, notably those reflecting maternal protectiveness. The findings of this study are discussed in relation to different hypothesized relationships between infant abuse and parenting style in macaques.

The evolution of male-infant interactions in the tribe Papionini (Primates: Cercopithecidae).

In Old World monkeys, intense affiliative interactions between adult males and infants have mostly been observed in the tribe Papionini. Although these male-infant interactions have been reported in most species of the genera Papio, Theropithecus and Cercocebus, they have only erratically been reported in the genus Macaca. In this article I show that the distribution of male-infant interactions within the genus Macaca can be accounted for by the phylogenetic relations among macaque species and by the evolution of the genus Macaca relative to the other Papionini.

Estradiol increases female sexual initiation independent of male responsiveness in rhesus monkeys.

Copulation and female initiation of sexual behavior vary across the ovarian cycle, suggesting that female hormonal condition influences female sexual motivation in rhesus monkeys. However, the effects of hormones on female sexual motivation are difficult to identify because male behavior also varies with female hormonal condition. During the nonbreeding season, male rhesus monkeys are sexually unresponsive to females; thus the effects of estradiol treatment on female sexual motivation can be examined independent of male behavior. This study administered estradiol to five ovariectomized females living in a large age-graded social group during the nonbreeding season. The behavior of these females with and without estradiol treatment was compared. Data were collected concurrently on five intact, noncycling, nonpregnant females. Estradiol treatment significantly increased sexual initiation by ovariectomized females toward males without any significant changes in male behavior. Estradiol-treated females also displayed greater sexual initiation than nonpregnant, intact females. Both estrogen and progesterone were important predictors of sexual initiation in females, with progesterone having an inhibitory effect. Endogenous progesterone levels in females were negatively correlated with male contact behavior, suggesting that female attractiveness is reduced by progesterone. This study provides further support for estrogen as the critical steroid increasing female sexual motivation in primates.

Child abuse and neglect: usefulness of the animal data.

This article reviews and critically discusses the relevance of animal data to research on child abuse and neglect. Although parental investment theory can be useful in investigating the adaptiveness, if any, of child abuse and neglect, the evolutionary approach also has some limitations. The most suitable animal models for investigating the psychosocial processes underlying child abuse and neglect are probably found among the nonhuman primates. Whereas the heuristic value of social deprivation paradigms may be limited, recent studies suggest that the spontaneous occurrence of infant maltreatment in monkeys may be the closest approximation to child maltreatment provided by nonhuman animals. The investigation of adaptive and maladaptive processes in the parenting behavior of socially living nonhuman primates can inform research on child abuse and neglect and allow investigators to conduct studies that would be difficult or impossible in humans.

Infant abuse and neglect in monkeys--a discussion of definitions, epidemiology, etiology, and implications for child maltreatment: reply to Cicchetti (1998) and Mason (1998)

In response to D. Cicchetti's (1998) and W. A. Mason's (1998) commentaries, this article scrutinizes infant maltreatment in monkeys and its public health implications. Studies of infant abuse and neglect in monkeys have used operational definitions based on (a) adult behavior or (b) adult behavior and infant outcome (depending on data available for analysis). Direct comparisons between the incidence of maltreatment in monkey and human populations can be only tentative as a result of differences in operational definitions of maltreatment. A simplified version of the ecological-transactional model of maltreatment can be used in research with nonhuman primates, and different species can be used to model different aspects of the human phenomenon. Although abuse and neglect take different forms in animals and humans, research with animal models can make an important contribution to elucidating the adaptive function, if any, of child maltreatment and the proximate mechanisms underlying its occurrence.

Maternal cradling and infant nipple preferences in rhesus monkeys (Macaca mulatta).

This study investigated lateral biases in nipple preferences, maternal cradling, carrying, and retrieval in 41 rhesus macaque (Macaca mulatta) mother-infant dyads living in two captive social groups. Observations were made during the first 6 weeks of infant life using a combination of scan sampling and ad-libitum sampling techniques. Infants exhibited a significant left-nipple preference in the first weeks of life but the bias decreased with infant age. Mothers showed a left-arm bias in carrying their infants but no significant lateral bias in cradling or retrieval. Our results suggest that the left-side cradling bias reported in studies of humans and some other primates reflects a bias in the infant's nipple preference rather than in maternal behavior. The infants' preference for the left nipple is consistent with both Salk's (1960) heartbeat hypothesis and with more recent hypotheses linking this lateral bias with brain asymmetry and hemispheric specialization for mother-infant communication.

Parenting styles of abusive mothers in group-living rhesus macaques

Maternal abuse of offspring in group-living monkeys was investigated to assess whether abuse of infants can be interpreted as an adaptive reduction of parental expenditure or as a behavioural pathology. I compared the parenting styles of 10 abusive and 10 non-abusive rhesus macaque, Macaca mulatta, mothers living in three large captive groups over the first 12 weeks of infant life. I also analysed the social interactions between mothers and infants and other individuals. Abusive females scored higher than controls on several measures of maternal protectiveness and rejection, indicating that they were highly controlling mothers. They also received fewer contacts and approaches from other individuals, and tended to be more aggressive and more interested in other females' infants compared to non-abusive mothers. Infant abuse was accompanied by similar or higher parental expenditure in the offspring rather than by a reduction in expenditure, as predicted by the adaptive hypothesis. Therefore, the results of this study support the hypothesis that infant abuse is a form of behavioural pathology. Infant abuse in rhesus macaques shows parallels with that in other primate species, but some of its characteristics could be a by-product of species-specific behavioural adaptations of rhesus macaques. Copyright 1998 The Association for the Study of Animal Behaviour.