Background

Evidence suggests that early life adversity is associated with maladaptive behaviors and is commonly an antecedent of stress-related psychopathology. This is particularly relevant to rearing in primate species as infant primates depend on prolonged, nurturant rearing by caregivers for normal development. To further understand the consequences of early life rearing adversity, and the relation among alterations in behavior, physiology and brain function, we assessed young monkeys that had experienced maternal separation followed by peer rearing with behavioral, endocrine and multimodal neuroimaging measures.

Methods

50 young rhesus monkeys were studied, half of which were rejected by their mothers and peer reared, and the other half were reared by their mothers. Assessments were performed at approximately 1.8 years of age and included: threat related behavioral and cortisol responses, cerebrospinal fluid (CSF) measurements of oxytocin and corticotropin releasing hormone (CRH), and multimodal neuroimaging measures (anatomical scans, resting functional connectivity, diffusion tensor imaging, and threat-related regional glucose metabolism).

Results

The results demonstrated alterations across behavioral, endocrine, and neuroimaging measures in young monkeys that were reared without their mothers. At a behavioral level in response to a potential threat, peer reared animals engaged in significantly less freezing behavior (p = 0.022) along with increased self-directed behaviors (p < 0.012). Levels of oxytocin in the CSF, but not plasma, were significantly reduced in the peer reared animals (p = 0.019). No differences in plasma cortisol or CSF CRH were observed. Diffusion tensor imaging revealed significantly decreased white matter density across the brain. Exploratory correlational and permutation analyses suggest that the impact of peer rearing on behavior, endocrine and brain structural alterations are mediated by separate parallel mechanisms.

Conclusions

Taken together, these results demonstrate in NHPs the importance of maternal rearing on the development of brain, behavior and hormonal systems that are linked to social functioning and adaptive responses. The findings suggest that the effects of maternal deprivation are mediated via multiple independent pathways which may account for the heterogeneity in behavioral and biological alterations observed in individuals that have experienced this early life adversity.

中文翻译：

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灵长类动物的早年逆境：行为、内分泌和神经影响

背景

有证据表明，早年的逆境与适应不良行为有关，并且通常是与压力相关的精神病理学的先兆。这与灵长类动物的饲养尤其相关，因为幼年灵长类动物的正常发育依赖于照顾者的长期养育。为了进一步了解生命早期养育逆境的后果，以及行为、生理和大脑功能改变之间的关系，我们通过行为、内分泌和多模式神经影像学测量，评估了经历过母亲分离、随后同伴养育的幼猴。

方法

研究人员对50 只年轻恒河猴进行了研究，其中一半被母亲拒绝并同伴饲养，另一半则由母亲饲养。评估在大约 1.8 岁时进行，包括：威胁相关的行为和皮质醇反应、脑脊液 (CSF) 催产素和促肾上腺皮质激素释放激素(CRH) 测​​量以及多模式神经影像测量（解剖扫描、静息功能连接、扩散张量成像） ，以及与威胁相关的区域葡萄糖代谢）。

结果

结果表明，在没有母亲的情况下饲养的幼猴的行为、内分泌和神经影像学指标发生了变化。在应对潜在威胁的行为水平上，同伴饲养的动物的冻结行为显着减少（p  = 0.022），同时自我导向行为增加（p  < 0.012）。在同伴饲养的动物中，脑脊液中的催产素水平显着降低，但血浆中的催产素水平没有显着降低（p  = 0.019）。未观察到血浆皮质醇或脑脊液 CRH 的差异。弥散张量成像显示整个大脑的白质密度显着降低。探索性相关和排列分析表明，同伴养育对行为、内分泌和大脑结构改变的影响是由单独的并行机制介导的。

结论

总而言之，这些结果在 NHP 中证明了母亲养育对与社会功能和适应性反应相关的大脑、行为和激素系统发育的重要性。研究结果表明，母性剥夺的影响是通过多种独立途径介导的，这可能解释了在经历过这种早年逆境的个体中观察到的行为和生物学改变的异质性。