Early Predictors of Impaired Social Functioning in Male Rhesus Macaques (Macaca mulatta)

Autism spectrum disorder (ASD) is characterized by social cognition impairments but its basic disease mechanisms remain poorly understood. Progress has been impeded by the absence of animal models that manifest behavioral phenotypes relevant to ASD. Rhesus monkeys are an ideal model organism to address this barrier to progress. Like humans, rhesus monkeys are highly social, possess complex social cognition abilities, and exhibit pronounced individual differences in social functioning. Moreover, we have previously shown that Low-Social (LS) vs. High-Social (HS) adult male monkeys exhibit lower social motivation and poorer social skills. It is not known, however, when these social deficits first emerge. The goals of this study were to test whether juvenile LS and HS monkeys differed as infants in their ability to process social information, and whether infant social abilities predicted later social classification (i.e., LS vs. HS), in order to facilitate earlier identification of monkeys at risk for poor social outcomes. Social classification was determined for N = 25 LS and N = 25 HS male monkeys that were 1–4 years of age. As part of a colony-wide assessment, these monkeys had previously undergone, as infants, tests of face recognition memory and the ability to respond appropriately to conspecific social signals. Monkeys later identified as LS vs. HS showed impairments in recognizing familiar vs. novel faces and in the species-typical adaptive ability to gaze avert to scenes of conspecific aggression. Additionally, multivariate logistic regression using infant social ability measures perfectly predicted later social classification of all N = 50 monkeys. These findings suggest that an early capacity to process important social information may account for differences in rhesus monkeys’ motivation and competence to establish and maintain social relationships later in life. Further development of this model will facilitate identification of novel biological targets for intervention to improve social outcomes in at-risk young monkeys.

自闭症谱系障碍（Autism Spectrum Disorder, ASD）以社交认知损害为特征，但其核心发病机制仍不甚明确。相关研究进展因缺乏能够呈现与ASD相关行为表型的动物模型而受阻。恒河猴（Rhesus Monkeys）是破解这一研究瓶颈的理想模式生物。与人类相似，恒河猴具有高度社会性，拥有复杂的社交认知能力，且在社会功能层面存在显著的个体差异。我们此前的研究已证实，低社交（Low-Social, LS）型成年雄性恒河猴相较于高社交（High-Social, HS）型个体，表现出更低的社交动机与更差的社交技能。但目前尚不清楚这些社交缺陷首次出现的时间节点。本研究旨在探究幼年低社交与高社交恒河猴在婴儿期处理社交信息的能力是否存在差异，同时验证婴儿期社交能力能否预测个体后续的社交分类（即低社交vs高社交），以期为更早识别存在不良社交结局风险的恒河猴提供支撑。本研究共纳入50只1至4岁的雄性恒河猴，其中低社交组、高社交组各25只。作为猴群整体评估的组成部分，这些个体在婴儿期曾接受面部识别记忆与对同种社交信号做出恰当反应的相关测试。后续被归类为低社交组与高社交组的恒河猴，在区分熟悉面孔与新奇面孔的能力，以及对同种攻击场景做出物种典型适应性凝视回避的能力上均存在缺陷。此外，基于婴儿期社交能力指标的多变量逻辑回归分析，可完美预测全部50只恒河猴的后续社交分类结果。本研究结果表明，早期处理关键社交信息的能力差异，或许可以解释恒河猴在成年后建立与维持社交关系的动机与能力差异。进一步优化这一动物模型，将有助于识别新型生物干预靶点，以改善存在社交风险的幼年恒河猴的社交结局。