Maternal hypothalamic-pituitary-adrenal axis response to foraging uncertainty: A model of individual vs. social allostasis and the "Superorganism Hypothesis"

Authors

Jeremy D. Coplan, SUNY Downstate Medical Center
Nishant K. Gupta, SUNY Downstate Medical Center
Asif Karim, SUNY Downstate Medical Center
Anna Rozenboym, CUNY Kingsborough Community CollegeFollow
Eric L.P. Smith, SUNY Downstate Medical Center
John G. Kral, SUNY Downstate Medical Center
Leonard A. Rosenblum, SUNY Downstate Medical Center

Document Type

Article

Publication Date

9-7-2017

Abstract

Introduction: Food insecurity is a major global contributor to developmental origins of adult disease. The allostatic load of maternal food uncertainty from variable foraging demand (VFD) activates corticotropin-releasing factor (CRF) without eliciting hypothalamic-pituitary-adrenal (HPA) activation measured on a group level. Individual homeostatic adaptations of the HPA axis may subserve second-order homeostasis, a process we provisionally term “social allostasis.” We postulate that maternal food insecurity induces a “superorganism” state through coordination of individual HPA axis response.

Methods: Twenty-four socially-housed bonnet macaque maternal-infant dyads were exposed to 16 weeks of alternating two-week epochs of low or high foraging demand shown to compromise normative maternal-infant rearing. Cerebrospinal fluid (CSF) CRF concentrations and plasma cortisol were measured pre- and post-VFD. Dyadic distance was measured, and blinded observers performed pre-VFD social ranking assessments.

Results: Despite marked individual cortisol responses (mean change = 20%) there was an absence of maternal HPA axis group mean response to VFD (0%). Whereas individual CSF CRF concentrations change = 56%, group mean did increase 25% (p = 0.002). Our "dyadic vulnerability" index (low infant weight, low maternal weight, subordinate maternal social status and reduced dyadic distance) predicted maternal cortisol decreases (p < 0.0001) whereas relatively “advantaged” dyads exhibited maternal cortisol increases in response to VFD exposure.

Comment: In response to a chronic stressor, relative dyadic vulnerability plays a significant role in determining the directionality and magnitude of individual maternal HPA axis responses in the service of maintaining a “superorganism” version of HPA axis homeostasis, provisionally termed “social allostasis.”

Comments

This article was originally published in PLOS One, available at DOI: 10.1371/journal. pone.0184340.

This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0).