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 initial weeks of life. This past year we further characterized face-to-face interactions between mothers and their newborn infants in a naturalistic setting. We reported large individual variability in rates of maternal/infant face-to-face interactions: first-time mothers engaged in mutual gazing/lip-smacking in the first 30 days of life significantly more than multiparous mothers, whereas the more experienced mothers let their infants out of their arms reach significantly more in the first 30 days of life than did primiparous mothers. Overall, mothers tended to engage in more face-to-face interactions with their male infants then with their infant daughters. We finished our initial investigation of brain activity during periods of imitation using scalp electrodes to record EEG activity, reporting 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 also 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 demonstrated similarities between infant human and infant monkey EEG during periods of imitation. We also compared neonatal imitation abilities in mother-reared (MR) and nursery-reared (NR) infants. MR infants responded to facial gestures earlier chronologically and with more gestures themselves over their first week, consistent with our previous EEG findings that MR infants show larger mu suppression than NR infants when viewing facial gestures during their initial days of life. Given the potential impact of neonatal imitation on infants' social, cognitive, and emotional development, we devised an intervention study in which NR infants either received additional facial gesturing from a human caretaker during their first month, 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. There were, however, some other benefits from the handling only treatment relative to the standard nursery rearing condition. Long-term follow-up observations revealed that the 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. Additional follow-up studies revealed that infants who received the early face interaction intervention exhibited more competent positive social behavior and lower levels of anxiety-related behaviors throughout the rest of their first year of life, relative to the monkeys in the other two 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 increased 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. Follow-up study of these infants revealed that oxytocin treatment improved social memory and gaze-following a month later, but only among male infants. 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. 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. We continued a project involving 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 Arizona State University, we collected milk samples from mothers over their infants' first 30 days of 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 and that mothers with higher hair cortisol during pregnancy had a higher MYE in the first 30 days of life. Importantly, we also 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 several additional studies published 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 living in a free-ranging outdoor environment. During the past year some major changes occurred in the population of free-ranging rhesus monkeys that had been maintained under relative stability with respect to social organization and existing dominance hierarchies for over a decade. The behavioral and biological consequences of these changes were documented using repeated measures of affiliative and agonistic behaviors collected several times per week, repeated measures of elo rankings every time a change in the groups dominance status was observed, and cortisol concentrations in blood and in hair samples collected quarterly. Major changes in all three sets of measures were documented following each demographic change, which consisted of (a) removal from the group (for veterinary purpose) of certain high-ranking individuals, the death of a non-alpha matriarch, and the removal of another non-alpha matriarch from another matrilineal family in the group, respectively. Analyses of epigenetic changes in genome-wide methylation patterns of lymphocytes obtained in the afore-mentioned blood samples are currently underway. We recently completed 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 overall 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.
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