Maternal buffering beyond glucocorticoids: impact of early life stress on corticolimbic circuits that control infant responses to novelty

• Authors: Brittany R. Howell, Emory University; Matthew S. McMurray, Emory University; Dora B. Guzman, Emory University; Govind Nair, Emory University; Yundi Shi, University of North Carolina; Kai M. McCormack, Emory University; Xiaoping P Hu, Emory University; Martin A. Styner, University of North Carolina; Mar Sanchez, Emory University
• Journal Title: Social Neuroscience
• Volume: Volume 12, Number 1
• Publisher: Taylor & Francis | 2017-01-01, Pages 50-64
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1080/17470919.2016.1200481
• Subjects: Health Sciences, Obstetrics and Gynecology; Psychology, Behavioral
• Keywords: Science & Technology; Social Sciences; Life Sciences & Biomedicine; Neurosciences; Psychology; Neurosciences & Neurology; Social buffering; maternal care; infant maltreatment; rhesus monkeys; uncinate fasciculus; CORTICOTROPIN-RELEASING HORMONE; WHITE-MATTER DEVELOPMENT; MACAQUES MACACA-MULATTA; LIVING RHESUS-MONKEYS; BEHAVIORAL-INHIBITION; CHILD MALTREATMENT; STRANGE SITUATION; EARLY EXPERIENCE; FIBER PATHWAYS; HPA AXIS

Abstract

Maternal presence has a potent buffering effect on infant fear and stress responses in primates. We previously reported that maternal presence is not effective in buffering the endocrine stress response in infant rhesus monkeys reared by maltreating mothers. We have also reported that maltreating mothers show low maternal responsiveness and permissiveness/secure-base behavior. Although still not understood, it is possible that this maternal buffering effect is mediated, at least partially, through deactivation of amygdala response circuits when mothers are present. Here, we studied rhesus monkey infants that differed in the quality of early maternal care to investigate how this early experience modulated maternal buffering effects on behavioral responses to novelty during the weaning period. We also examined the relationship between these behavioral responses and structural connectivity in one of the underlying regulatory neural circuits: amygdala-prefrontal pathways. Our findings suggest that infant exploration in a novel situation is predicted by maternal responsiveness and structural integrity of amygdala-prefrontal white matter depending on maternal presence (positive relationships when mother is absent). These results provide evidence that maternal buffering of infant behavioral inhibition is dependent on the quality of maternal care and structural connectivity of neural pathways that are sensitive to early life stress.