How Gene-Environment Interactions Shape Biobehavioral Development: Lessons From Studies With Rhesus Monkeys

Recent research has found marked individual differences in patterns of rhesus monkey biobehavioral development throughout the life span. Approximately 20% of monkeys growing up in naturalistic settings consistently display unusually fearful and anxious-like behavioral reactions to novel, mildly stressful social situations throughout development; another 5%-10% are likely to exhibit impulsive and/or inappropriately aggressive responses under similar circumstances. These distinctive behavioral patterns and their biological correlates appear early in life and remain remarkably stable from infancy to adulthood. Both genetic and experiential mechanisms are implicated not only in the expression of these patterns but also in their transmission across successive generations of monkeys. For example, a specific polymorphism in the serotonin transporter gene is associated with deficits in infant neurobehavioral functioning and in juvenile and adolescent control of aggression and serotonin metabolism in monkeys that experienced insecure early attachments but not in monkeys that developed secure attachment relationships with their mothers during infancy (maternal buffering). Moreover, because the attachment style of a monkey mother is typically "copied" by her daughters when they grow up and become mothers themselves, similar buffering is likely to occur for the next generation of infants carrying that specific polymorphism.     

Social and nonsocial behaviors of adult rhesus monkeys after amygdalectomy in infancy or adulthood.

At 6 yr of age six female rhesus monkeys that had sustained bilateral amygdalectomy in infancy, and five intact controls, were transferred to an observation cage where behaviors were recorded while the monkeys were (a) alone, (b) paired with unfamiliar stimulus animals, and (c) paired with familiar monkeys from the opposite experimental group. The five adult controls then underwent amygdalectomy, and all tests were repeated with the infant- and adult-operated animals. Infant-operated monkeys changed behaviors more rapidly than did intact controls in social and nonsocial situations, and their activity levels were less modified after a 24-hr period in the observation cage. They were subordinate to intact controls but expressed less fear than did controls when briefly placed with an unfamiliar aggressive animal. Adult amygdalectomy produced many changes in behavior, but these aberrations were identical to those observed in like-age monkeys that had been amygdalectomized in infancy. Infant-operated monkeys demonstrated more behavioral deficits at 6 yr than they had earlier in life.     

Continuity in social cognition from infancy to childhood

Research examining the development of social cognition has largely been divided into two areas: infant perception of intentional agents, and preschoolers’ understanding of others’ mental states and beliefs (theory of mind). Many researchers have suggested that there is continuity in social cognitive development such that the abilities observed in infancy are related to later preschool ability, yet little empirical evidence exists for this claim. Here, we present preliminary evidence that capacities specific to the social domain contribute to performance in social cognition tasks both during infancy and in early childhood. Specifically, looking time patterns in an infant social cognition task correlated with preschool theory of mind; however, no such relationship was found for infants in a nonsocial cognition task.     

Targets,tactics, and the open mouth face during play fighting in three species of primates

The play fighting of many mammals involves the nonserious use of behavior patterns derived from serious fighting. A major question of theoretical importance has been that of how, given this overlap in patterns of behavior, the animals can distinguish between playful and nonplayful intent. One proposed solution is that animals use play signals to inform each other about the playful intent of their actions. The most widely reported play signal amongst primates is the open mouth play face. The manner in which this so-called signal functions is based on correlational evidence, with most reports simply noting its presence or absence in a given species. This study involved a detailed video-based analysis of the occurrence of open mouths during the play fighting of three species of primates. One captive troop each of ring-tailed lemurs, black-handed spider monkeys, and patas monkeys was used. By examining all open mouths in the context of the species-typical style of play fighting, several conclusions were empirically verified. 1) Most open mouths occur as a functionally necessary precursor for biting. 2) Some open mouths occur as a defensive threat which deters further contact. 3) The residual open mouths which may function as contact promoting play signals, constituted about 20–25% of all open mouths by the lemurs and patas monkeys, but less than 5% for spider monkeys. These species differences appeared to arise from two causes. Firstly, the spider monkeys used another signal, the head shake, in situations where lemurs and patas monkeys used open mouths. Secondly, the style of play fighting greatly influenced the frequency and duration of open mouths. This was most marked in the face-to-face combat style of patas monkeys. These findings show that comparative studies of the occurrence and function of play signals need to take into account species-typical styles of playful combat. Aggr. Behav. 23:41–57, 1997. © 1997 Wiley-Liss, Inc.     

The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals

The natural pedagogy hypothesis proposes that human infants preferentially attend to communicative signals from others, facilitating rapid cultural learning. In this view, sensitivity to such signals is a uniquely human adaptation and as such nonhuman animals should not produce or utilize these communicative signals. We test these evolutionary predictions by examining sensitivity to communicative cues in 206 rhesus monkeys (Macaca mulatta) using an expectancy looking time task modeled on prior work with infants. Monkeys observed a human actor who either made eye contact and vocalized to the monkey (social cue), or waved a fruit in front of her face and produced a tapping sound (nonsocial cue). The actor then either looked at an object (referential look) or looked toward empty space (look away). We found that, unlike human infants in analogous situations, rhesus monkeys looked longer at events following nonsocial cues, regardless of the demonstrator's subsequent looking behavior. Moreover younger and older monkeys showed similar patterns of responses across development. These results provide support for the natural pedagogy hypothesis, while also highlighting evolutionary changes in human sensitivity to communicative signals.     

When girls versus boys play alone: nonsocial play and adjustment in kindergarten.

The goal of the present study was to examine the relations between different forms of children's nonsocial play behaviors and adjustment in kindergarten. The participants in this study were 77 kindergarten children (38 boys, 39 girls; mean age = 66.16 months, SD = 4.11 months). Mothers completed ratings of child shyness and emotion dysregulation. Children's nonsocial play behaviors (reticent, solitary-passive. solitary active) were observed during free play. In addition, teachers rated child behavior problems (internalizing and externalizing) and social competence; academic achievement was assessed through child interviews. Results from regression analyses revealed that different types of nonsocial play were differentially associated with child characteristics and indices of adjustment. For some forms of nonsocial play, the nature of these associations differed significantly for boys and girls.     

Peer-peer interaction among infants and toddlers with extensive daycare experience

Peer-peer interaction among 10–21- and 24–30-month-olds with extensive daycare experience was studied. Thirteen pairs of familiar agemates were formed, and each dyad was observed in a playpen with toys at their daycare center. Adult preparation and various constraints to peer-peer interaction were minimized. The nine behavioral measures included nonsocial, marginally social, and social play categories. The results revealed equivalent amounts of nonsocial behavior for both age groups, and marginally social behavior was not the dominant play activity at either age. Compared with the younger group, the older children engaged in less marginally social activity, more positive social behavior overall, and more sustained sociable interchanges. Neither age group had high levels of antisocial behavior, but the younger children tended to display more than the older. Support was found for the view that marginally social activity functions as a bridge from nonsocial to social behavior.     

Social touch alters newborn monkey behavior

In humans, infants respond positively to slow, gentle stroking—processed by C-tactile (CT) nerve fibers—by showing reductions in stress and increases in eye contact, smiling, and positive vocalizations. More frequent maternal touch is linked to greater activity and connectivity strength in social brain regions, and increases children’s attention to and learning of faces. It has been theorized that touch may prime children for social interactions and set them on a path towards healthy social cognitive development. However, less is known about the effects of touch on young infants’ psychological development, especially in the newborn period, a highly sensitive period of transition with rapid growth in sensory and social processing. It remains untested whether newborns can distinguish CT-targeted touch from other types of touch, or whether there are benefits of touch for newborns’ social, emotional, or cognitive development. In the present study, we experimentally investigated the acute effects of touch in newborn monkeys, a common model for human social development. Rhesus macaques (Macaca mulatta), like humans, are highly social, have complex mother-infant interactions with frequent body contact for the first weeks of life, making them an excellent model of infant sociality. Infant monkeys in the present study were reared in a neonatal nursery, enabling control over their early environment, including all caregiver interactions. One-week-old macaque infants (N = 27) participated in three 5-minute counter-balanced caregiver interactions, all with mutual gaze: stroking head and shoulders (CT-targeted touch), stroking palms of hands and soles of feet (Non-CT touch), or no stroking (No-touch). Immediately following the interaction, infants watched social and nonsocial videos and picture arrays including faces and objects, while we tracked their visual attention with remote eye tracking. We found that, during the caregiver interactions, infants behaved differently while being touched compared to the no-touch condition, irrespective of the body part touched. Most notably, in both touch conditions, infants exhibited fewer stress-related behaviors—self-scratching, locomotion, and contact time with a comfort object—compared to when they were not touched. Following CT-targeted touch, infants were faster to orient to the picture arrays compared to the other interaction conditions, suggesting CT-targeted touch may activate or prime infants’ attentional orienting system. In the No-touch condition infants attended longer to the nonsocial compared to the social video, possibly reflecting a baseline preference for nonsocial stimuli. In contrast, in both touch conditions, infants’ looked equally to the social and nonsocial videos, suggesting that touch may influence the types of visual stimuli that hold infants’ attention. Collectively, our results reveal that newborn macaques responded positively to touch, and touch appeared to influence some aspects of their subsequent attention, although we found limited evidence that these effects are mediated by CT fibers. These findings suggest that newborn touch may broadly support infants’ psychological development, and may have early evolutionary roots, shared across primates. This study illustrates the unique insight offered by nonhuman primates for exploring early infant social touch, revealing that touch may positively affect emotional and attentional development as early as the newborn period.     

Conditional catecholamine changes in rhesus monkeys

Magnitude of changes in levels of plasma norepinephrine and epinephrine from basal levels was compared in four rhesus monkeys upon presentations of positive and of negative conditional stimuli (CS + and CS ?) during sessions of Pavlovian fear conditioning. The two monkeys providing the least information as to when shock would be delivered both showed significantly increased levels of epinephrine during CS + sessions. Following a course of extinction trials, these differences disappeared. Changes in levels of plasma norepinephrine were not as consistent, possibly because of the fact that only limited amounts of this neurohumor find their way into the circulation. The data demonstrate that neurohumors with a very brief half-life can be conditioned. Moreover, since the amount of shock used was the same for the two subgroups studied, the data on epinephrine levels are consistent with our hypothesis that environmental factors other than the physical stimulus itself may play a role in habituation of a visceral response. Data from behavioral studies would suggest that this occurs because the animal learns when it is safe or in danger.     

Cognitive style: problem solving by rhesus macaques (Macaca mulatta) reared with living or inanimate substitute mothers

Cognitive style, reflected in the generation of novel solutions and the use of identifiable response strategies in problem-solving situations, was contrasted in rhesus monkeys (Macaca mulatta) reared individually with either canine companions or inanimate surrogate mothers. Four experiments were conducted over a 5-year period, examining problem solving in relatively unstructured as well as more formal situations. Results indicated that whereas the 2 rearing groups did not differ on most measures of performance, consistent response strategies were identified for the dog-raised monkeys. The results were compared with previously published data from the same monkeys demonstrating rearing group differences in abilities to engage in complex social interaction. The animate nature of the early rearing environment may facilitate-the development of a cognitive style that influences problem-solving abilities in both the social and nonsocial realms.     

The persistence of some effects of handling in infancy on the behaviour of the adult rat

An attempt was made to discover how persistent the effects of handling before weaning are on activity, grooming, emotional elimination and learning in adult rats; whether there is an interaction of the effects of handling and the effects of cage size on the behaviour of rats; and whether the daily removal of the mother during nursing has any effects on the pups.

Since all differences between handled and undisturbed animals found at 50 or 100 days were found at 220 days, it was concluded that the effects of handling in infancy are persistent. The hypothesis that cage size and removal of the mother during nursing significantly affect adult behaviour was not supported by the results.     

To look or not to look: an eye movement study of hypervigilance during change detection in high and low spider fearful students

Previous eye movement studies of attentional bias in spider fear reported inconsistent results with respect to early attentional capture, suggesting that overt attentional capture only reliably occurs under specific circumstances. In addition, none of these studies explored covert attention. The present study examined attentional bias in spider phobia using a change detection paradigm that was expected to provide good conditions for documenting attentional capture. In contrast to our expectations, eye movement data showed that all participants' first fixations were fastest on general negative targets, whereas participants' first fixations on spider targets were slower in the spider fearful than in the nonfearful group. In addition, spider fearful participants made more nontarget fixations before fixating on a spider target than did nonfearful participants. Thus, we found that participants' overt attention was more quickly focused on general negative targets, whereas covert attentional processes enabled initial avoidance of fear-relevant (i.e. spider) stimuli. The present findings have important implications for research on attention and fear as they indicate that fearful individuals are not characterized by static attentional orienting toward threat but, under certain conditions, may avert attention from threat automatically.     

Plasma glucose and insulin levels in monkeys anticipating feeding

To see whether plasma glucose or insulin changed in anticipation of feeding, we provided seven rhesus monkeys with four-hour access to food every other day. Blood was sampled before and during a 30-minute signal which ended with food availability and before and during a 30-minute signal which was not closely and reliably linked with food availability. Plasma insulin showed no evidence of conditioning. Plasma glucose was higher during the signal than prior to the signal in both experiments. This probably reflects the arousing nature of the signal rather than appetitive-associated learning. However, the differences, while statistically significant, were probably biologically trivial because they fall within the normal fluctuations of meal-fed monkeys. Under the conditions of this experiment, it appears that conditional changes in glucose and insulin do not reliably occur in monkeys anticipating access to food.     

Play fighting and the development of agonistic behavior in male and female rats

Two longitudinal studies were conducted to quantify the social behaviors exhibited by both male and female Long-Evans rats from the immediate postweaning period until young adulthood. In Experiment 1, male sibling pairs engaged in a high level of play fighting during the early juvenile period but such activity declined to a level significantly lower than that of female and mixed-sex pairs after 54 days of age. In Experiment 2, social exchanges during maturation were examined during the presence and absence of the piloerection response in an effort to distinguish play fighting from agonistic interactions. In male pairs, piloerection was rarely seen before 55–75 days of age but thereafter occurred with increasing frequency especially among dominant males. Furthermore, subordinate males retreated from their dominant partners and remained in an escape chamber for a significant amount of time only during encounters involving the exhibition of piloerection. This finding suggests that piloerection can be useful in identifying play and aggressive interactions. In female and heterosexual pairs, piloerection was observed infrequently during social encounters occurring throughout maturation. In addition, when given the opportunity to escape, females were less likely to retreat from play activity if their partner was another female than a male.     

Contingency experiences of 3-month-old children and their relation to later developmental achievements

In this study, the authors investigated the relation between early social contingency experiences and infants' competencies to detect nonsocial contingencies. In this study of 87 three-month-old infants, the authors operationalized early social contingencies as prompt, contingent maternal responses and coded microanalytically on the basis of video-recorded mother-infant interactions. The authors assessed competence to detect nonsocial contingencies by 2 methods: (a) the mobile conjugate reinforcement paradigm, which focuses on detecting contingencies between the infants' actions (kicking) and nonsocial consequences (mobile moving) and (b) the visual expectation paradigm, which focuses on detecting contingencies between 1 event (a smiley face projected on a screen) that was followed by a 2nd event (a complex picture projected on the other side of the screen). The results showed that early social contingencies are related to the competency to detect nonsocial action-consequence contingencies in the mobile conjugate reinforcement paradigm.     

Temperament and play interaction behavior across infancy

Temporal stability and convergent validity of infant temperament ratings and play interaction behaviors were examined across early to late infancy. Stability was noted for the temperament dimensions activity, rhythmicity, intensity, mood, and persistence. Stability also was noted for the infant play interaction behaviors looking, smiling, and vocalizing. In addition, convergent validity was noted for attentive-affective behaviors and comparable temperament ratings; for example, gaze aversion and nondistractability, and distress brow behavior and negative mood. Generally easier temperament infants were noted to vocalize more and to cry less frequently during their play interactions.     

Targets and tactics of agonistic and precopulatory behavior in montane and prairie voles: Their relationship to juvenile play-fighting

Play-fighting by juvenile montane and prairie voles involves attack and defense of the head, neck and shoulders. Since during play animals typically borrow behavior patterns from other functional contexts, two adult behavioral contexts were compared to juvenile play-fighting. These were serious fighting and sexual encounters. During serious fighting in a resident-intruder paradigm, most bites are directed at the rump and lower flanks. During sexual encounters, especially in precopulatory behavior, the head, neck and shoulders are gently contacted. Therefore, play-fighting by juveniles would appear to involve attack and defense of areas of the body contacted in adult precopulatory behavior, not adult fighting. Furthermore, the species-specific differences in juvenile play-fighting were also found to be matched by species-specific differences in precopulatory behavior. In both playful and precopulatory encounters, montane voles contacted the head and used upright defensive behaviors more often than prairie voles. In contrast, prairie voles made mutual contact more often and were more likely to rotate to supine in defense of contact to the nape and head. These findings support our hypothesis that juvenile play-fighting in muroid rodents involves the precocial expression of precopulatory, not agonistic behavior.     

Spider fearful individuals attend to threat, then quickly avoid it: evidence from eye movements

According to cognitive models of anxiety, anxiety patients exhibit an early reflexive attentional bias toward threat stimuli, which may be followed by intentional avoidance of these stimuli. To determine the time course of attentional vigilance and avoidance, the authors conducted an eye-tracking study in which 22 highly spider fearful participants (SFs) and 23 nonanxious control participants (NACs) studied groups of 4 pictures (spider, butterfly, dog, and cat). The authors found that the very first fixation was on a spider picture more often in SFs than in NACs. However, SFs quickly moved their eyes away from the spider they had fixated first, yielding shorter gaze durations than NACs. Afterward, SFs exhibited shorter gaze durations on spiders than NACs for the rest of the 1-min presentation time. This early reflexive attentional bias toward threat followed by avoidance of threat may explain earlier failures to find attentional biases in anxiety.     

The relation of children's everyday nonsocial peer play behavior to their emotionality, regulation, and social functioning

The relations of children's nonsocial behavior to their emotionality, regulation, and social functioning were examined in a short-term longitudinal study. Parents (primarily mothers) and teachers rated children's effortful regulation, emotionality, asocial behaviors, problem behaviors, and social acceptance, and children's nonsocial play behaviors were observed for two semesters. Peers also rated likability. Children's observed reticent activities were related to adults' ratings of high regulation, low externalizing problems, and high asocial behavior, as well as to low anger and low positive emotion. On the other hand, solitary play was associated with low positive emotion and low regulation over time and with high asocial behavior and high peer exclusion. Peer rejection mediated the relation of internalizing emotions (anxiety, low positive emotion) and regulation to solitary play later in the school year, and asocial play mediated the relation of internalizing emotions to both solitary and reticent play behavior.