This past year we followed up on our initial study of rhesus monkey infant's capacity to imitate specific facial expressions directed toward them by a human model in their initial days of life. Such early imitative capabilities have been reported for human neonates, and they are thought to be reflexively mediated by mirror neurons, a recently characterized class of visual-motor neurons found in ventral premotor and parietal cortex. We found that some (but not all) of the newborns tested were able to mimic specific facial expressions involving differential mouth and tongue movements, but not until their second or third day of life. Follow-up behavioral observations revealed that infants who exhibited imitative behavior during their first week of life subsequently exhibited significantly higher levels of social play during peer interactions sessions from 4 months onward than those infants who failed to imitate during their first week. Moreover, when these monkeys were subsequently permanently moved into large groups of same-age peers, those individuals who had failed to imitate during their initial days of life exhibited much higher levels of self directed behaviors than those who did, and they also displayed repeated bouts of autistic-like repetitive stereotypic behavior, something that was never observed in any of the monkeys who had demonstrated imitative capabilities as neonates. This past year, in collaboration with colleagues from the University of Maryland, we also developed a procedure to monitor EEG activity in the monkey infants throughout the imitative test sessions, as well as during appropriate non-imitative control periods. Initial analyses have revealed that (a) it is possible to reliably obtain EEG data relatively unobtrusively from newborn rhesus infants in this test setting, and (b) there appear to be specific patterns of slow-way EEG activity concomitant with imitative behavior that seem consistent with those previously found to accompany mirror neuron activity in adult macaques and that are not seen in infants who fail to imitate in the same setting. ? ? This year we published the results of a long-term prospective longitudinal study examining the relationship between CSF 5-HIAA concentrations and life-history outcomes in male rhesus living in a free-ranging environment on Morgan Island, SC. Previous work had demonstrated a significant inverse relationship between CSF 5-HIAA concentrations and levels of aggression during the juvenile and adolescent years in this field population, replicating findings obtained in laboratory studies, and a positive relationship between 5-HIAA concentrations and both age of male natal troop emigration and likelihood of survival with increasing age. Results of the present analyses extended some previous findings and qualified others. First, as in previous laboratory studies, individual differences CSF 5-HIAA concentrations were exceedingly stable from pre-adolescence into the adult years: Males who had relatively high 5-HIAA concentrations at 2-3 years of age continued to have high levels at 10 years of age and beyond; males with low 5-HIAA concentrations as juveniles continued to have low levels in subsequent years as well.? Second, as previously reported, low CSF 5-HIAA concentrations early in life were associated with early mortality but only for males who emigrated from their natal troop prior to puberty. A few males with low CSF 5-HIAA concentrations as juveniles stayed in their natal troop well past puberty before they eventually emigrated and their post-emigration mortality rate was relatively low. Interestingly, virtually all of these late-emigrating low 5-HIAA males were offspring of females from socially dominant families within the natal troop. Thus it appears that in natural settings high family social status may represent a powerful protective factor for rhesus monkey males whose patterns of aggressive behavior and serotonin metabolism otherwise put them at high risk for early mortality.? ? This year we also tested the efficacy of a new design for a fleece-covered surrogate """"""""mother"""""""" for our nursery-reared rhesus monkey infants. Unlike traditional surrogates that are spring-mounted from a base resting on the floor of the infant's cage, the new surrogates hang from the top of the cage, not only affording greater movement in more dimensions than the traditional model but also giving the infant greater control of the surrogate's movements. We found that infants reared on the hanging surrogates exhibited a stronger grasping response, greater motor coordination, earlier spontaneous crawling, and better balance during their initial month, more exploratory behavior in their home cage, and more time away from their surrogate and lower salivary cortisol levels when placed in a novel setting, compared to infants reared on traditional surrogates. As a result of these findings, we are now replacing the standard surrogates with the hanging model in our nursery. In addition, we demonstrated the efficacy of a retractable perch for more effective utilization of cage space in both individually- and group-housed monkeys of multiple ages. In collaboration with colleagues from the University of Massachusetts, Amherst, we also collected multiple samples of hair from monkeys of different ages, rearing backgrounds, current housing conditions, and differing social status to be assayed for cortisol levels as a potential index of chronic stress, and we compared those values with cortisol levels repeatedly obtained from saliva during the extended periods between hair sampling of the same monkeys and with behavioral observations collected concomitantly. Our initial analyses indicate that this measure holds considerable promise as a reliable index of individual differences in chronic stress, at least in the monkeys sampled to date. ? ? Finally, this past year we published seveal studies utilizing the CBGS's colony of tufted capuchin monkeys. One study revealed that preferences for specific food items in restricted choice situations appears to be motivated more by the experience of frustration than by aversion resulting from perceived social inequality. A second study showed that capuchin monkeys are not able to use a mirror to touch marks on their body not visible without the mirror, a standard test of self-recognition in human infants and several other primate species, even when they have been previously trained to touch marks that are visible. A third study documented that urine washing in this species was not influenced by relative temperature and humidity and hence seems unlikely to have a thermoregulatory function, as has been the consensus hypothesis to date, but rather appears to have specific social functions for individuals of differing gender and social status.
| Ruggiero, Angela M; Novak, Matthew F S X; Woodward, Ruth A et al. (2009) Successful behavioral strategy to unite mother and infant rhesus monkeys (Macaca mulatta) after cesarean delivery. Am J Primatol 71:510-22 |
| Byrne, Gayle; Suomi, Stephen J (2009) Intimate social behavior in infant interactions in Cebus apella. Am J Primatol 71:77-85 |
| Miller, Kimran E; Laszlo, Katalin; Suomi, Stephen J (2008) Why do captive tufted capuchins (Cebus apella) urine wash? Am J Primatol 70:119-26 |
| Novak, Matthew Fsx; Kenney, Caroline; Suomi, Stephen J et al. (2007) Use of animal-operated folding perches by rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 46:35-43 |
| Lutz, Corrine K; Davis, Ernie B; Ruggiero, Angela M et al. (2007) Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta). Am J Primatol 69:584-90 |
| Roma, Peter G; Silberberg, Alan; Huntsberry, Mary E et al. (2007) Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks. Am J Primatol 69:989-1000 |
| Roma, Peter G; Champoux, Maribeth; Suomi, Stephen J (2006) Environmental control, social context, and individual differences in behavioral and cortisol responses to novelty in infant rhesus monkeys. Child Dev 77:118-31 |
| Roma, Peter G; Silberberg, Alan; Ruggiero, Angela M et al. (2006) Capuchin monkeys, inequity aversion, and the frustration effect. J Comp Psychol 120:67-73 |
| Silberberg, Alan; Roma, Peter G; Ruggiero, Angela M et al. (2006) On inequity aversion in nonhuman primates. J Comp Psychol 120:76 |
| Suomi, Stephen J (2005) Aggression and social behaviour in rhesus monkeys. Novartis Found Symp 268:216-22; discussion 222-6, 242-5 |
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