Human 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 e. More detailed subsequent observations revealed that during this time mother-infant dyads were communicating via complex forms of emotional exchanges, including exaggerated lip-smacking and sustained mutual gaze. 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, which indicated a sophisticated capacity to control and flexibly engage in affective communication. For those infants who could imitate in this fashion, this capability was evident on their first postnatal day, although their imitative behavior largely disappeared after the first week. Interestingly, we found major rearing condition differences in imitative capabilities: whereas approximately 55% of nursery-reared infants could imitate, over 90% of mother-reared infants were successful imitators. Follow-up studies of infants who displayed imitative capabilities during their first week vs. those who did not revealed that imitators performed better on tests of sensory-motor capabilities throughout their first month, played twice as much as non-imitators from 4 to 6 months of age, and whereas a sizable number of non-imitators developed idiosyncratic, autistic-like stereotypic behaviors during their second year, none of the monkeys who had displayed imitative behavior their first week exhibited any such stereotypies. Recent studies have suggested that human infants exert active control over imitative responses and provoke previously imitated gestures even after a delay of up to 24 h. Delayed imitation is regarded as the hallmark of a sophisticated capacity to control and flexibly engage in affective communication and has been described as an indicator of innate protoconversational readiness. However, we are not the only primates to exhibit neonatal imitation, and delayed imitation abilities may not be uniquely human. This past year we reported that 1-week-old rhesus monkey infants who showed immediate imitation of a lipsmacking gesture also showed delayed imitation of lipsmacking, facilitated by a tendency to refrain from lipsmacking toward a still face during baseline measurements. Individual differences in delayed imitation suggest that differentially matured cortical mechanisms may be involved, allowing some newborns macaques to actively participate in communicative exchanges from birth. Thus, rhesus monkey infants are endowed with basic social competencies of intersubjective communication that indicate cognitive and emotional commonality between humans and macaques, which may have evolved to nurture an affective mother-infant relationship in primates. We have also been investigated 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. This past year we reported that the results of these experiments revealed a distinctive EEG signature involving significant suppression of mu rhythm activity at low frequencies in frontal and parietal brain regions during periods of imitation but not during baseline and control periods and not in monkeys who failed to imitate. 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. Our data show that the 57 Hz frequency band responds reliably to changes in illumination. As well, we found EEG in higher frequencies (1220 Hz) that 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). Finally, this past year we published two studies utilizing our colony of tufted capuchin monkeys (C apella). The first study focused on fur-rubbing behavior. This behavior is widely believed to have a social bonding function in capuchin monkeys, yet a recent study of tufted capuchins revealed increased levels of aggression and reduced levels of affiliation after fur-rubbing bouts. This observed decrease in group cohesion may be attributable to increased intragroup competition for fur-rub material rather than being a direct effect of fur rubbing itself. To test this hypothesis, we separated individual tufted monkeys (Cebus apella) from their social group and provided them with fur-rub material or control material, thereby avoiding intragroup competition. After engagement with materials, we released subjects back into their social group and observed their subsequent interactions with group members. We found that subjects were more likely to encounter aggression and less likely to receive affiliation from others in the fur-rub condition than in the control condition. These results support the idea that fur rubbing carries social after-effects for capuchin monkeys. The second study focused on the relationships among cognittive performance, emotional state, and stress hormone levels. Abnormal stereotypic behavior is widespread among captive non-human primates and is generally associated with jeopardized well-being. However, attributing the same significance to all of these repetitive, unvarying and apparently functionless behaviors may be misleading, as some behaviors may be better indicators of stress than others. Previous studies have demonstrated that the affective state of the individual can be inferred from its bias in appraising neutral stimuli in its environment. Therefore, in the present study, in order to assess the emotional state of stereotyping individuals, 16 captive tufted capuchins (Cebus apella) were tested on a judgment bias paradigm and their faecal corticoid levels were measured in order to assess the intensity of the emotional state. Capuchins with higher levels of stereotypic head twirls exhibited a negative bias while judging ambiguous stimuli and had higher levels of fecal corticoids compared to subjects with lower levels of head twirls. Levels of stereotypic pacing, however, were not correlated with the monkeys emotional state. This study is the first to reveal a positive correlation between levels of stereotypic behaviour and a pessimistic-like judgment bias in a non-human primate by employing a recently developed cognitive approach. Combining cognitive tests that evaluate the animals affective valence (positive or negative) with hormonal measurements that provide information on the strength of the emotional state conduces to a better understanding of the animals affective state and therefore to their well-being.

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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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