Human mothers interact emotionally with their newborns through exaggerated facial expressions and mutual gaze, a capacity that has long been considered uniquely human. We previously 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 of life. This past year we further characterized face-to-face interactions between mothers and their newborn infants in a naturalistic setting. We found large individual variability in rates of maternal/infant face-to-face interactions, in that mothers who had only one or two infants engaged in mutual gazing/lipsmacking in the first 30 days of life significantly more than mothers who had had three or more infants,whereas the more experienced mothers let their infants out of their arms reach significantly more in the first 30 days of life than newer mothers. Overall, mothers tended to engage in more face-to-face interactions with their male infants. 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 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. We reported that this pattern of EEG activity intensified through that first week, and it was significantly stronger in mother-reared than in nursery-reared neonates. These findings demonstrate similarities between infant human and infant monkey EEG during periods of imitation. We also 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. We reported that 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 one 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 showed increased preference for a social video at D30 and again at D40, had better memory for social stimuli when tested at D60, and had higher levels of social contact with peers from D40 to D60,compared to infants in the handling and standard rearing groups. A second intervention designed to increase infants social perception and social sensitivity looked at the effects of oxytocin on infants social interactions. NR infants were nebulized with oxytocin or saline, and were then tested in an imitation recognition task. We reported inncreased time spent looking at faces following oxytocin, but not saline, treatment. Salivary assays confirmed increased levels of oxytocin, and infants also 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 faces of conspecifics, which suggests a genetic predisposition towards rhesus faces in particular. We also reported that particular sensitivities towards the eye region are exhibited by neonatal imitators but not by non-imitators, which may indicate that neonatal imitation and differential social sensitivity are intricately linked. A project begun last 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 collected milk samples from mothers over their infants' first 30 days of her infants life, and we analyzed these samples for cortisol content and nutrient composition. Similar to Dr. Hinde's studies of human mothers milk in older infants, we found that parity predicted milk yield volume (MYE) in the first month of life. Our findings also indicated that mothers with higher hair cortisol during pregnancy had a higher MYE in the first 30 days of life. Additionally, we found that cortisol levels in mothers' milk predicted infant cognitive functioning and social behavior later in life. Infants who ingested milk with higher cortisol content were less impulsive of a cognitive task but also initiated social behaviors with peers less frequently. Hair cortisol was used as a measure of chronic HPA activity in 3 additional studies completed this past year. First, hair cortisol levels shortly after birth, presumably reflecting prenatal HPA activity from mid-gestation onward, predicted cognitive performance capabilities and infant temperament in the first postnatal months. Second, changes in hair cortisol concentrations during the juvenile years predicted differences in social dominance status among adult female monkeys. A third project centered on the incidence of alopecia and related physiological processes. We had 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 we examined the role of chronic HPA axis activity as assessed by hair cortisol concentrations in alopecia. Our early results indicate that overall concentrations change across pregnancy and that monkeys that exhibit the greatest amount of hair loss have higher hair cortisol concentrations than those that do not. We continued our research program on personality and facial characteristics with our capuchin monkeys, focusing on 5 personality dimensions (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness, and reported that the monkeys facial width-to-height ratio as well as their face w), and found that the 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. This past year we also provided some of our capuchins with stone tools and observed for the first time in our colony spontaneous use of those tools to crack open walnuts. Nut-cracking has been observed in a few isolated wild populations of this species but is clearly far from universal. We plan to study its pattern of propagation in our captive colony, especially among juvenile and adolescent group members.
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