Abstract
Chronic stress may conceivably require plasticity of maternal physiology and behavior to cope with the conflicting primary demands of infant rearing and foraging for food. In addition, social rank may play a pivotal role in mandating divergent homeostatic adaptations in cohesive social groups. We examined cerebrospinal fluid (CSF) oxytocin (OT) levels and hypothalamic-pituitary adrenal (HPA) axis regulation in the context of maternal social stress and assessed the contribution of social rank to dyadic distance as reflective of distraction from normative maternal-infant interaction. Twelve socially housed mother-infant bonnet macaque dyads were studied after variable foraging demand (VFD) exposure compared to 11 unstressed dyads. Dyadic distance was determined by behavioral observation. Social ranking was performed blindly by two observers. Post-VFD maternal plasma cortisol and CSF OT were compared to corresponding measures in non-VFD-exposed mothers. High-social rank was associated with increased dyadic distance only in VFD-exposed dyads and not in control dyads. In mothers unexposed to VFD, social rank was not related to maternal cortisol levels, whereas VFD-exposed dominant versus subordinate mothers exhibited increased plasma cortisol. Maternal CSF OT directly predicted maternal cortisol only in VFD-exposed mothers. CSF OT was higher in dominant versus subordinate mothers. VFD-exposed mothers with "high" cortisol specifically exhibited CSF OT elevations in comparison to control groups. Pairing of maternal social rank to dyadic distance in VFD presumably reduces maternal contingent responsivity, with ensuing long-term sequelae. VFD-exposure dichotomizes maternal HPA-axis response as a function of social rank with relatively reduced cortisol in subordinates. OT may serve as a homeostatic buffer during maternal stress exposure.
Highlights
Exposure to early-life stress increases susceptibility to the development of, among other conditions, mood and anxiety disorders in humans [1, 2]
We examined the role of cerebrospinal fluid oxytocin (CSF OT) in the context of maternal social stress, social rank, and hypothalamic–pituitary adrenal (HPA)-axis regulation
There was no relationship between infant age and maternal–infant distance, maternal social rank, maternal plasma cortisol, or maternal CSF OT (p > 0.6 for all correlations)
Summary
Exposure to early-life stress increases susceptibility to the development of, among other conditions, mood and anxiety disorders in humans [1, 2]. Because of a shared primate ancestry with humans, as well as similarity to humans by virtue of complexity in social structure, affective expression, genetic similarity, and maternal–infant bonding patterns [3], non-human primates provide a cogent model to facilitate understanding of the neurobiological underpinnings of certain forms of human psychiatric disorders as related to early-life stress exposure [4, 5]. Variable foraging demand (VFD) is an experimental model of early-life stress that manipulates maternal accessibility to food in a social environment, putatively disrupting maternal–infant dyadic attachment and creating unpredictable rearing conditions for non-human primate infants [8]. We examined cerebrospinal fluid (CSF) oxytocin (OT) levels and hypothalamic–pituitary adrenal (HPA) axis regulation in the context of maternal social stress and assessed the contribution of social rank to dyadic distance as reflective of distraction from normative maternal–infant interaction
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