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Developmental outcomes of early adverse care on amygdala functional connectivity in nonhuman primates

Published online by Cambridge University Press:  11 January 2021

Elyse L. Morin ,
Brittany R. Howell ,
Eric Feczko ,
Eric Earl ,
Melanie Pincus ,
Katherine Reding ,
Zsofia A. Kovacs-Balint ,
Jerrold S. Meyer ,
Martin Styner  and
Damien Fair
...Show all authors
Elyse L. Morin
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
Brittany R. Howell
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA Fralin Biomedical Research Institute at VTC, Roanoke, VA, USA Department of Human Development and Family Science, Virginia Tech, Blacksburg, VA, USA
Eric Feczko
Affiliation:
Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
Eric Earl
Affiliation:
Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
Melanie Pincus
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
Katherine Reding
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA
Zsofia A. Kovacs-Balint
Affiliation:
Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
Jerrold S. Meyer
Affiliation:
Department of Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, USA
Martin Styner
Affiliation:
Departments of Psychiatry and Computer Science, University of North Carolina, Chapel Hill, NC, USA
Damien Fair
Affiliation:
Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
Mar M. Sanchez*
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
*
Author for Correspondence: Dr. Mar Sanchez, Department of Psychiatry and Behavioral Sciences, and Yerkes National Primate Research Center, Emory University, 954 Gatewood Drive NE, NS 4216, Atlanta, GA30329; E-mail: [email protected].
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Abstract

Despite the strong link between childhood maltreatment and psychopathology, the underlying neurodevelopmental mechanisms are poorly understood and difficult to disentangle from heritable and prenatal factors. This study used a translational macaque model of infant maltreatment in which the adverse experience occurs in the first months of life, during intense maturation of amygdala circuits important for stress and emotional regulation. Thus, we examined the developmental impact of maltreatment on amygdala functional connectivity (FC) longitudinally, from infancy through the juvenile period. Using resting state functional magnetic resonance imaging (MRI) we performed amygdala–prefrontal cortex (PFC) region-of-interest and exploratory whole-brain amygdala FC analyses. The latter showed (a) developmental increases in amygdala FC with many regions, likely supporting increased processing of socioemotional-relevant stimuli with age; and (b) maltreatment effects on amygdala coupling with arousal and stress brain regions (locus coeruleus, laterodorsal tegmental area) that emerged with age. Maltreated juveniles showed weaker FC than controls, which was negatively associated with infant hair cortisol concentrations. Findings from the region-of-interest analysis also showed weaker amygdala FC with PFC regions in maltreated animals than controls since infancy, whereas bilateral amygdala FC was stronger in maltreated animals. These effects on amygdala FC development may underlie the poor behavioral outcomes associated with this adverse experience.

Keywords

amygdala functional connectivitychildhood maltreatmentearly life stressprefrontal cortexrhesus monkey
Type
Special Section 1: 2019 Minnesota Symposium on Child Psychology
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1579 - 1596
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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