Adaptation Of Laboratory Reared Monkeys To Field Environments

在过去的一年里，我们扩大了对恒河猴新生儿在出生后最初一周内模仿人类模型对他们的特定面部表情的能力的调查。这种早期的模仿能力在人类新生儿中已经被报道过，他们被认为最初是由镜像神经元反射性地介导的。我们发现，在接受测试的托儿所喂养的新生儿中，大约60%的人能够模仿特定的面部表情，包括拍打嘴唇和伸出舌头等不同的面部表情，但他们的模仿能力在10天大时基本消失。在出生后第一个月的跟踪行为观察显示，在第一周表现出模仿行为的婴儿随后在目标定向运动(例如，伸手和抓住物体)和精细的手运动控制方面比没有模仿者表现出更多的技能，这可能反映了顶叶和运动皮质中运动链的不同成熟，这与镜像神经元系统部分重叠(5)。与马里兰大学的同事合作，我们还监测了新生儿在整个模仿测试过程中以及在适当的非模仿控制期内的脑电活动。在他们出生后的第一周，初步分析揭示了伴随模仿行为的慢波EEGα去同步的特定模式，但在其他条件下和在相同环境中未能模仿的婴儿中看不到，这再次与镜像神经元参与这些现象的解释一致。 在过去的一年里，我们还扩大了对恒河猴出生后最初几天母婴互动的研究。与之前关于该物种依恋关系规范发展的报道形成鲜明对比的是，我们发现恒河猴母婴二元在其生命的前三周进行频繁而密集的面对面互动，之后这些模式基本上消失。有趣的是，这种消失的发育时间在很大程度上与婴儿开始自愿中断与母亲的身体接触的时期相吻合，因为他们开始探索外部的物理和社会环境(4)。我们还证明了恒河猴婴儿从出生第一天起就能区分猴子面孔的图片和非社会刺激，到第10天，在没有出生后接触任何性别的成年人的情况下，他们表现出对成年雌性猴子面孔图片的显著偏好。 与马萨诸塞大学阿默斯特分校的同事合作，我们收集了不同类别猕猴的多个毛发样本，以测试皮质醇浓度作为慢性应激的潜在指标，我们发现了显著的年龄、性别和社会地位差异：较年轻、雌性和较低级别的猴子的毛皮质醇浓度高于较年长、较雄性和较高级别的个体。我们还将这些值与分别从圈养的Tonkean猕猴(M.tokeana)和巴巴里猕猴(M.Silvana)的圈养群体中获得的皮质醇样本进行了比较，每一种猕猴都保存在类似的室外围栏中。Tonkean猕猴表现出与恒河猴相同的年龄、性别和地位差异，但总体上它们的皮质醇水平显著高于它们的同类猕猴；相反，Barbary猕猴的毛皮质醇浓度一直低于它们的同类猕猴，这可能反映了这三个不同物种之间整体社会优势结构和相对攻击水平的差异。另一项研究表明，恒河猴婴儿头发皮质醇浓度的差异可靠地预测了在各种认知发展指标上的表现差异：皮质醇水平较高的婴儿需要更长时间才能达到皮亚吉特物体持久性任务的标准(3)。 最后，在过去的一年里，我们发表了几项研究，利用我们的簇毛卷尾猴(C Apella)。一项里程碑式的研究表明，卷尾猴能够识别何时被人类观察者模仿，这种模仿导致它们更喜欢模仿它们的观察者，而不是那些不模仿它们的观察者(9)。相反，另一项研究发现卷尾猴没有表现出以前在恒河猴、猿和人类身上表现出的相同的记忆意识模式(1)。第三项研究调查了卷尾猴在定位隐藏食物时使用不同感官信息的情况，发现它们在这种努力中始终使用视觉信息，而不是听觉信息(7)。另一项研究对婴儿和少年卷尾猴表现出的面对面和其他亲密的社交互动进行了表征，发现这些活动大多不是针对它们的母亲，而是涉及它们社会群体的其他成员(2)，这与恒河猴婴儿和它们的母亲之间激烈的面对面互动形成了鲜明的对比(4)。另一方面，卷尾猴幼年在与同伴的社交游戏的形式和数量上表现出显著的性别差异，这与之前报道的包括人类在内的其他灵长类物种的性别差异完全一致。

This past year we expanded our investigation of the capacity of rhesus monkey neonates to imitate specific facial expressions directed toward them by a human model throughout their initial week of life. Such early imitative capabilities have been reported for human neonates, and they are thought to be initially reflexively mediated by mirror neurons. We found that approximately 60% of nursery-reared newborns tested were able to mimic specific facial expressions involving different facial expressions such as lip-smacking and tongue protrusion but that their imitative capacity largely disappeared by 10 days of age. Follow-up behavioral observations throughout the first month of life revealed that infants who had exhibited imitative behavior during their first week subsequently displayed significantly more developed skills in goal-directed movements (e.g., reaching for and grasping objects) and fine hand motor control than non-imitators, possibly reflecting differential maturation of motor chains in the parietal and motor cortices, which partially overlap with the mirror neuron system (5). In collaboration with colleagues from the University of Maryland, we also monitored EEG activity in the neonates throughout their imitative test sessions, as well as during appropriate non-imitative control periods, during their first postnatal week, Preliminary analyses revealed specific patterns of slow-wave EEG alpha desynchronization concomitant with imitative behavior, but not under other conditions and not seen in infants who failed to imitate in the same setting, again consistent with an interpretation of mirror neuron involvement in these phenomena. This past year we also expanded our study of rhesus monkey mother-infant interactions during the initial postnatal days. In marked contrast to previous reports concerning the normative development of attachment relationships in this species, we found that rhesus monkey mother- infant dyads engage in frequent and intensive face-to-face interactions throughout their first 3 weeks of life, after which those patterns largely disappear. Interestingly, the developmental timing of this disappearance largely coincides with the period when infants begin to voluntarily break physical contact with their mother as they start exploring their external physical and social environment (4). We also demonstrated the rhesus monkey infants can differentiate pictures of monkey faces from nonsocial stimuli from Day 1 onward and that by Day 10 they show a significant preference for pictures of adult female monkey faces over those of adult males in the absence of any postnatal exposure to adults of either gender. In collaboration with colleagues from the University of Massachusetts, Amherst, we collected multiple samples of hair from different groups of rhesus monkeys in order to assay for cortisol concentrations as a potential index of chronic stress, and we found significant age, gender, and social status differences: younger, female, and low-ranking monkeys had higher hair cortisol concentrations than older, male and high-ranking individuals. We also compared these values with hair cortisol samples obtained from captive colonies of Tonkean macaques (M. tokeana) and Barbary macaques (M. silvana), respectively, each maintained in a similar outdoor enclosures. The Tonkean macaques exhibited the same pattern of age, gender, and status differences that characterized the rhesus groups, but overall their cortisol levels were significantly higher than those of their rhesus counterparts; in contrast, the hair cortisol concentrations for the Barbary macaques were consistently lower than those of their rhesus counterparts, possibly reflecting differences in the overall social dominance structure and relative levels of aggression among these 3 different macaque species. Another study demonstrated that differences in hair cortisol concentrations among rhesus monkey infants reliably predicted differences in performance on a variety of measures of cognitive development: infants with higher cortisol levels took longer to reach criterion on Piagetian object permanence tasks (3). Finally, this past year we published several studies utilizing our colony of tufted capuchin monkeys (C apella). A landmark study demonstrated that capuchin monkeys are capable of recognizing when they are being imitated by a human observer and that such imitation leads them to prefer observers who imitate them to those who do not (9). Another study, in contrast, found that capuchin monkeys fail to exhibit the same pattern of memory awareness previously demonstrated in rhesus monkeys, apes, and humans (1). A third study investigated the use of different sensory information by capuchin monkeys when locating hidden food items and found that they consistently utilize visual but not auditory information in such endeavors (7). Another study characterized face-to-face and other intimate social interactions exhibited by infant and juvenile capuchin monkeys and found that most of these activities were directed not toward their mother but instead involved other members of their social group (2), in marked contrast to the intense face-to-face interactions between rhesus infants and their mothers (4). On the other hand, capuchin monkey juveniles exhibit significant gender differences in the form and amount of social play with peers that were completely consistent with those previously reported for other primate species, including humans (8).