Effects of social subordination and oestradiol on resting-state amygdala functional connectivity in adult female rhesus monkeys

• Type of Material: Article
• Authors: Katherine M. Reding, Emory University; David S. Grayson, University of California, Davis; Oscar Miranda-Dominguez, Oregon Health and Science University; Siddarth Ray, Oregon Health and Science University; Mark Wilson, Emory University; Donna Toufexis, Emory University; Damien A. Fair, Oregon Health and Science University; Maria Sanchez, Emory University
• Language: English
• Date: 2020-02-11
• Publisher: WILEY
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: 2020
• Final Published Version (URL): http://dx.doi.org/10.1111/jne.12822
• Title of Journal or Parent Work: JOURNAL OF NEUROENDOCRINOLOGY
• Volume: 32
• Issue: 2
• Start Page: e12822
• End Page: e12822
• Grant/Funding Information: The studies were supported by NIH grants MH81816 (DT), MH81816-S1 (DT), P50 MH078105-04S1 (MMS), and Yerkes National Primate Research Center Base Grant P51OD011132. The Yerkes NPRC is fully accredited by AAALAC International.
• Keywords: Endocrinology & Metabolism; stress; oestradiol; Neurosciences & Neurology; CHRONIC STRESS; SEX-DIFFERENCES; MEDIAL PREFRONTAL CORTEX; ESTROGEN-RECEPTOR-ALPHA; MESSENGER-RNA EXPRESSION; STREPSIRHINE PRIMATE GALAGO; rhesus monkey; resting-state; VISUAL-CORTEX; GRANULAR FRONTAL-CORTEX; Neurosciences; fMRI; Science & Technology; CORTICAL CONNECTIONS; TRANSPORTER GENE MODIFY; Life Sciences & Biomedicine
• Research Categories: Biology, Neuroscience; Biology, Animal Physiology

Abstract

Preclinical studies demonstrate that chronic stress modulates the effects of oestradiol (E2) on behaviour through the modification of the amygdala and the medial prefrontal cortex (mPFC) neuronal structure. Clinical studies suggest that alterations in amygdala functional connectivity (FC) with the mPFC may be associated with stress-related phenotypes, including mood and anxiety disorders. Thus, identifying the effects of stress and E2 on amygdala-mPFC circuits is critical for understanding the neurobiology underpinning the vulnerability to stress-related disorders in women. In the present study, we used a well-validated rhesus monkey model of chronic psychosocial stress (subordinate social rank) to examine effects of E2 on subordinate (SUB) (i.e. high stress) and dominant (DOM) (i.e. low stress) female resting-state amygdala FC with the mPFC and with the whole-brain. In the non-E2 treatment control condition, SUB was associated with stronger left amygdala FC to subgenual cingulate (Brodmann area [BA] 25: BA25), a region implicated in several psychopathologies in people. In SUB females, E2 treatment strengthened right amygdala-BA25 FC, induced a net positive amygdala-visual cortex FC that was positively associated with frequency of submissive behaviours, and weakened positive amygdala-para/hippocampus FC. Our findings show that subordinate social rank alters amygdala FC and the impact of E2 on amygdala FC with BA25 and with regions involved in visual processing and memory encoding.