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其生命的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研究。这种早期的模仿能力已经在人类新生儿中被报道过，并且它们被认为最初是由镜像神经元反射性地介导的。我们发现，大约60%的接受测试的托儿所养育的新生儿能够模仿特定的面部表情，包括不同的面部表情，如舔嘴唇和舌头伸出，但他们的模仿能力在10天大的时候基本上消失了。 在出生后的第一个月进行的后续行为观察显示，在第一周表现出模仿行为的婴儿随后在目标导向运动方面表现出明显更发达的技能（例如，达到和抓住物体）和精细的手部运动控制比非模仿者，可能反映了顶叶和运动皮质中运动链的差异成熟，这与镜像神经元系统部分重叠（5）。与来自马里兰州大学的同事合作，我们还监测了新生儿在整个模仿测试期间的EEG活动，以及在适当的非模仿控制期间，在他们出生后的第一周，初步分析显示了与模仿行为相伴的慢波EEG α去兴奋化的特定模式，但在其他条件下则没有，在同样的环境下无法模仿的婴儿中也没有，这再次与镜像神经元参与这些现象的解释相一致。 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相互作用的研究。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对在其生命的前3周内进行频繁和密集的面对面互动，之后这些模式基本消失。有趣的是，这种消失的发育时间在很大程度上与婴儿开始主动中断与母亲的身体接触的时期相吻合，因为他们开始探索他们的外部物理和社会环境（4）。我们还证明了恒河猴婴儿可以区分猴子的脸从非社会刺激的图片从第1天起，到第10天，他们表现出显着的偏好成年女性猴子的脸在没有任何出生后暴露于成年男性的照片。 我们与马萨诸塞州大学的同事合作，从不同的恒河猴群体中收集了多个毛发样本，以测定皮质醇浓度作为慢性压力的潜在指标，我们发现了显著的年龄，性别和社会地位差异：年轻，女性和低级别的猴子比年长，男性和高级别的个体有更高的毛发皮质醇浓度。我们还比较了这些值与毛发皮质醇样本获得圈养殖民地的通肯猕猴（M。tokeana）和巴巴利猕猴（M. Silicon），各自保持在类似的室外外壳中。通肯猕猴表现出与恒河猴群体相同的年龄、性别和地位差异模式，但总体而言，它们的皮质醇水平显著高于恒河猴;相比之下，巴巴利猕猴的毛发皮质醇浓度始终低于恒河猴，这可能反映了这三种不同猕猴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，恒河猴婴儿毛发皮质醇浓度的差异可靠地预测了各种认知发展指标的表现差异：皮质醇水平较高的婴儿需要更长的时间才能达到皮亚杰客体恒存任务的标准（3）。 最后，在过去的一年里，我们发表了几项利用我们的簇绒卷尾猴（C apella）群体的研究。一项具有里程碑意义的研究表明，卷尾猴能够识别人类观察者何时模仿它们，这种模仿使它们更喜欢模仿它们的观察者而不是那些不模仿它们的人（9）。相反，另一项研究发现，卷尾猴未能表现出与先前在恒河猴，猿和人类中证明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的食物时使用不同的感官信息，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）。另一项研究描述了婴儿和少年卷尾猴表现出的面对面和其他亲密的社会互动，并发现这些活动中的大多数不是针对他们的母亲，而是涉及他们社会群体的其他成员（2），与恒河猴婴儿和他们的母亲之间激烈的面对面互动形成鲜明对比（4）。另一方面，卷尾猴幼猴在与同龄人的社交游戏形式和数量方面表现出显着的性别差异，这与先前报道的其他灵长类物种（包括人类）完全一致（8）。

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).