nHuman mothers interact emotionally with their newborns through exaggerated facial expressions and mutual gaze, a capacity that has long been considered uniquely human. A few years ago we initiated a research program on early face-to-face interactions in rhesus monkeys after we had serendipitously discovered that very young rhesus monkey infants did, in fact, engage in extensive face-to-face interactions with their mothers, but only during their first month or so of life. This past year we characterized face-to-face interactions between mothers and their newborn infants in a naturalistic setting. We found, similar to our previous results from mother-infant pairs housed in social pens, large individual variability in rates of maternal/infant face-to-face interactions. Further analysis revealed that newer mothers who had only one or two infants engaged in mutual gazing/lipsmacking in the first 30 days of life significantly more than more experienced mothers with three or more infants. Conversely, the more experienced mothers let their infants out of their arms reach significantly more in the first 30 days of life than newer mothers. We also discovered that during their first week some (but not all) infants could accurately match certain facial gestures produced by a human experimenter, even after a delay. For those infants who could imitate in this fashion, this capability was evident on their first postnatal day. We have since been investigating brain activity during periods of imitation vs. exposure to a dynamic but nonsocial stimulus (a rotating disk) and during non-stimulus baseline periods, using scalp electrodes to record EEG activity, and found a distinctive EEG signature involving significant suppression of mu rhythm activity at low frequencies in frontal and parietal brain regions exclusively during periods of imitation. This pattern of EEG activity intensified through that first week, and it was significantly stronger in mother-reared than in nursery-reared neonates. We also documented the emergence of EEG rhythms in one-week-old infant rhesus macaques under both light and dark conditions, showing that the 57 Hz frequency band responds reliably to changes in illumination and that EEG in higher frequencies (1220 Hz)significantly increase between dark and light conditions, similar to the increase in the beta band of humans during cognitive tasks. These findings demonstrate similarities between infant human and infant monkey EEG. More recently, we have demonstrated, using eye-tracking technology, that week-old infants readily respond to a computer-generated dynamic monkey avatar, and that those infants who imitate tend to focus on different aspects of the aviatars face (eyes and mouth) than those don't (mouth only). We also compared neonatal imitation abilities in mother-reared and nursery-reared monkeys, focusing on D3 performance only. Even though NR infants show an imitation effect when tested over the first week, they do not exhibit imitation specifically on D3. In contrast, MR monkeys responded to facial gestures with more gestures themselves, consistent with our previous EEG findings that MR infants show larger mu suppression than NR infants when viewing facial gestures. Given the potential impact of neonatal imitation on infants'social, cognitive, and emotional development, we devised an intervention whereby NR infants either received additional facial gesturing from a human caretaker, received additional handling (but did not see facial gestures), or remained in standard nursery rearing. We found that only the group that had received facial gesturing showed improved performance on the standard neonatal imitation task on D7 and showed greater sensitivity to facial identity of others in a standardized stranger task. Infants from the facial gesturing group also appear to be less inhibited in their latency to touch a toy in a novel object task and had better memory for social stimuli compared to infants in the handling and standard nursery rearing groups. A second attempt to increase infants social perception and social sensitivity looked at the effects of oxytocin on infants social interactions. Nursery-reared infants were nebulized with oxytocin or saline, and were then tested in an imitation recognition task. Salivary assays confirmed increased levels of oxytocin, and infants showed increased affiliative gesturing towards a human experimenter following oxytocin administration. We further explored infants facial processing strategies by presenting them with various faces and facial configurations on a remote eye tracker. Rhesus macaque infants generally prefer faces with normally arranged features over faces with linearly arranged featured, suggesting a special sensitivity to faces and face-like stimuli. These preferences are particularly strong for rhesus rather than human faces, which furthermore indicates a genetic predisposition towards rhesus faces in particular. We also found particular sensitivities towards the eye region in neonatal imitators but not in non-imitators, which may indicate that neonatal imitation and differential social sensitivity are intricately linked. A new project begun this year has involved the analysis of mothers milk in rhesus monkeys with respect to parity and early life history (i.e., rearing condition). In collaboration with Dr. Katie Hinde at Harvard University, we have begun collecting milk samples from mothers within the first 30 days of her infants life, and we are currently analyzing these samples for cortisol content and nutrient composition. Dr. Hinde has examined mothers milk for infants aged 3-4 months and has found that mothers yield milk of differing quality and quantity based on the sex of the her offspring. At this age, cortisol in mothers milk is also predictive of infant temperament. At the LCE, we are in the unique position to study, for the first time, similar relationships in neonatal milk (the first 30 days of life). Similar to Dr. Hindes studies of mothers milk in older infants, we have found that parity predicts milk yield volume (MYE) in the first month of life. Our preliminary findings also indicate that mothers with higher hair cortisol during pregnancy have a higher MYE in the first 30 days of life. We are currently examining this relationship with respect to both the mothers and infants hair cortisol reflective of long-term HPA axis activity in the neonatal period. We are further examining the extent to which constituents in mothers milk (cortisol and nutrient content) during the neonatal period influence infant social behavior, cognitive development, and temperament. Another focus is on the incidence of alopecia and related physiological processes. We have previously observed that many females undergo severe hair loss during pregnancy, only to regain full hair growth in the two months postpartum. In collaboration with Drs. Novak and Meyer at U-Mass, we are examining the role of chronic HPA axis activity as assessed by hair cortisol concentrations in alopecia. Our early results indicate that overall concentrations change across pregnacy and that monkeys that exhibit hair loss have higher hair cortisol concentrations than those that do not. We stared a research program on personality and facial characteristics with our Cebus monkeys, ide 5 personality dimensions (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness), and found that Cebus monkeys facial width-to-height ratio as well as their face w), and found that Cebus monkeys facial width-to-height ratio as well as their face width/lower face height are positively and significantly associated with Assertiveness. Lower face/face height ratio was also associated with neuroticism and attentiveness, suggesting that facial morphology reflects personality domains.

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Wooddell, Lauren J; Kaburu, Stefano Sk; Suomi, Stephen J et al. (2017) Elo-rating for Tracking Rank Fluctuations after Demographic Changes Involving Semi-free-ranging Rhesus Macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 56:260-268
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
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
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 :
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
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
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; Kaburu, Stefano S K; Byers, Kristen L et al. (2016) First-time rhesus monkey mothers, and mothers of sons, preferentially engage in face-to-face interactions with their infants. Am J Primatol 78:238-46
Dettmer, Amanda M; Kaburu, Stefano S K; Simpson, Elizabeth A et al. (2016) Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys. Nat Commun 7:11940
Kaburu, Stefano S K; Paukner, Annika; Simpson, Elizabeth A et al. (2016) Neonatal imitation predicts infant rhesus macaque (Macaca mulatta) social and anxiety-related behaviours at one year. Sci Rep 6:34997

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