This past year we expanded our investigation of the capacity of rhesus monkey neonates to imitate specific facial expressions directed toward them by a human model throughout their initial week of life. Such early imitative capabilities have been reported for human neonates, and they are thought to be initially reflexively mediated by mirror neurons. We found that approximately 60% of nursery-reared newborns tested were able to mimic specific facial expressions involving different facial expressions such as lip-smacking and tongue protrusion but that their imitative capacity largely disappeared by 10 days of age. Follow-up behavioral observations throughout the first month of life revealed that infants who had exhibited imitative behavior during their first week subsequently displayed significantly more developed skills in goal-directed movements (e.g., reaching for and grasping objects) and fine hand motor control than non-imitators, possibly reflecting differential maturation of motor chains in the parietal and motor cortices, which partially overlap with the mirror neuron system (5). In collaboration with colleagues from the University of Maryland, we also monitored EEG activity in the neonates throughout their imitative test sessions, as well as during appropriate non-imitative control periods, during their first postnatal week, Preliminary analyses revealed specific patterns of slow-wave EEG alpha desynchronization concomitant with imitative behavior, but not under other conditions and not seen in infants who failed to imitate in the same setting, again consistent with an interpretation of mirror neuron involvement in these phenomena. This past year we also expanded our study of rhesus monkey mother-infant interactions during the initial postnatal days. In marked contrast to previous reports concerning the normative development of attachment relationships in this species, we found that rhesus monkey mother- infant dyads engage in frequent and intensive face-to-face interactions throughout their first 3 weeks of life, after which those patterns largely disappear. Interestingly, the developmental timing of this disappearance largely coincides with the period when infants begin to voluntarily break physical contact with their mother as they start exploring their external physical and social environment (4). We also demonstrated the rhesus monkey infants can differentiate pictures of monkey faces from nonsocial stimuli from Day 1 onward and that by Day 10 they show a significant preference for pictures of adult female monkey faces over those of adult males in the absence of any postnatal exposure to adults of either gender. In collaboration with colleagues from the University of Massachusetts, Amherst, we collected multiple samples of hair from different groups of rhesus monkeys in order to assay for cortisol concentrations as a potential index of chronic stress, and we found significant age, gender, and social status differences: younger, female, and low-ranking monkeys had higher hair cortisol concentrations than older, male and high-ranking individuals. We also compared these values with hair cortisol samples obtained from captive colonies of Tonkean macaques (M. tokeana) and Barbary macaques (M. silvana), respectively, each maintained in a similar outdoor enclosures. The Tonkean macaques exhibited the same pattern of age, gender, and status differences that characterized the rhesus groups, but overall their cortisol levels were significantly higher than those of their rhesus counterparts;in contrast, the hair cortisol concentrations for the Barbary macaques were consistently lower than those of their rhesus counterparts, possibly reflecting differences in the overall social dominance structure and relative levels of aggression among these 3 different macaque species. Another study demonstrated that differences in hair cortisol concentrations among rhesus monkey infants reliably predicted differences in performance on a variety of measures of cognitive development: infants with higher cortisol levels took longer to reach criterion on Piagetian object permanence tasks (3). Finally, this past year we published several studies utilizing our colony of tufted capuchin monkeys (C apella). A landmark study demonstrated that capuchin monkeys are capable of recognizing when they are being imitated by a human observer and that such imitation leads them to prefer observers who imitate them to those who do not (9). Another study, in contrast, found that capuchin monkeys fail to exhibit the same pattern of memory awareness previously demonstrated in rhesus monkeys, apes, and humans (1). A third study investigated the use of different sensory information by capuchin monkeys when locating hidden food items and found that they consistently utilize visual but not auditory information in such endeavors (7). Another study characterized face-to-face and other intimate social interactions exhibited by infant and juvenile capuchin monkeys and found that most of these activities were directed not toward their mother but instead involved other members of their social group (2), in marked contrast to the intense face-to-face interactions between rhesus infants and their mothers (4). On the other hand, capuchin monkey juveniles exhibit significant gender differences in the form and amount of social play with peers that were completely consistent with those previously reported for other primate species, including humans (8).

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Slonecker, Emily M; Simpson, Elizabeth A; Suomi, Stephen J et al. (2018) Who's my little monkey? Effects of infant-directed speech on visual retention in infant rhesus macaques. Dev Sci 21:
Festante, Fabrizia; Vanderwert, Ross E; Sclafani, Valentina et al. (2018) EEG beta desynchronization during hand goal-directed action observation in newborn monkeys and its relation to the emergence of hand motor skills. Dev Cogn Neurosci 30:142-149
Damon, Fabrice; Méary, David; Quinn, Paul C et al. (2017) Preference for facial averageness: Evidence for a common mechanism in human and macaque infants. Sci Rep 7:46303
Dettmer, Amanda M; Rosenberg, Kendra; Menard, Mark T et al. (2017) Differential relationships between chronic hormone profiles in pregnancy and maternal investment in rhesus monkey mothers with hair loss in the neonatal period. Am J Primatol 79:1-8
Dettmer, Amanda M; Murphy, Ashley M; Guitarra, Denisse et al. (2017) Cortisol in Neonatal Mother's Milk Predicts Later Infant Social and Cognitive Functioning in Rhesus Monkeys. Child Dev :
Wooddell, Lauren J; Hamel, Amanda F; Murphy, Ashley M et al. (2017) Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys. Psychoneuroendocrinology 84:109-115
Simpson, Elizabeth A; Paukner, Annika; Sclafani, Valentina et al. (2017) Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques. Psychopharmacology (Berl) 234:497-506
Simpson, Elizabeth A; Jakobsen, Krisztina V; Damon, Fabrice et al. (2017) Face Detection and the Development of Own-Species Bias in Infant Macaques. Child Dev 88:103-113
Dettmer, Amanda M; Wooddell, Lauren J; Rosenberg, Kendra L et al. (2017) Associations between early life experience, chronic HPA axis activity, and adult social rank in rhesus monkeys. Soc Neurosci 12:92-101
Paukner, Annika; Wooddell, Lauren J; Lefevre, Carmen E et al. (2017) Do capuchin monkeys (Sapajus apella) prefer symmetrical face shapes? J Comp Psychol 131:73-77

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