Adaptation Of Laboratory Reared Monkeys To Field Environments

在过去的一年里，我们对恒河猴婴儿在生命最初的日子里模仿人类模型所指示的特定面部表情的能力进行了初步研究。这种早期的模仿能力已经在人类新生儿中得到了报道，并且它们被认为是由镜像神经元反射性地介导的，镜像神经元是最近在腹侧运动前皮层和顶叶皮层中发现的一类视觉运动神经元。我们发现，一些（但不是全部）接受测试的新生儿能够模仿特定的面部表情，包括不同的嘴和舌头运动，但直到他们出生的第二或第三天。后续行为观察显示，在出生后第一周表现出模仿行为的婴儿，在4个月后的同伴互动中，比那些在第一周没有模仿的婴儿表现出更高的社交游戏水平。此外，当这些猴子随后被永久地转移到一大群同龄的同伴中时，那些在生命最初的日子里没有模仿的猴子比那些模仿的猴子表现出更高水平的自我指导行为，而且它们还表现出反复发作的自闭症样的重复刻板行为，这在任何在新生儿时表现出模仿能力的猴子身上都没有观察到。在过去的一年里，我们与马里兰大学的同事合作，开发了一种程序来监测猴子婴儿在整个模仿测试过程中的脑电图活动，以及在适当的非模仿控制期间。初步分析显示：(a)在这种测试环境下，可以相对不显眼地从新生恒河猴婴儿那里可靠地获得脑电图数据；(b)似乎存在伴随模仿行为的慢速脑电图活动的特定模式，这似乎与之前在成年恒河猴身上发现的伴随镜像神经元活动的模式一致，而在相同环境下没有模仿的婴儿身上没有看到。

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.