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

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.

KEYWORDS:

• Social buffering
• maternal care
• infant maltreatment
• rhesus monkeys
• uncinate fasciculus

Acknowledgements

Special thanks to Anne Glenn, Christine Marsteller, Jennifer Miles, and all of the staff at the Yerkes National Primate Research Center (YNPRC) Field Station and Imaging Center.

We would also like to thank the members of the NIMH-funded “Early Experience, Stress and Neurobehavioral Development Center” (P50 MH078105), particularly the PI (Megan Gunnar) for the stimulating discussions of the data presented here. We also appreciate the statistical guidance we received from Chris Desjardins and Melinda Higgins during these analyses. This research was supported by NIMH grants MH078105, MH086203, and MH015755, NICHD grant HD055255, and Office of Research Infrastructure Programs/OD grant OD11132 (YNPRC Base grant, formerly RR000165). The content is solely the responsibility of the authors and does not represent the official views of the NIMH, NICHD or the NIH. The YNPRC is fully accredited by the Association for the Assessment and Accreditation of Laboratory Care, International.

Disclosure statement

No potential conflict of interest was reported by the authors.

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Additional information

Funding

This work was supported by the National Institute of Child Health and Human Development [HD055255]; National Institute of Mental Health [F31 MH086203], [P50 MN078105], [T32MH015755]; Office of Research Infrastructure Programs/OD [P51 OD11132].