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Edited by Michael I. Posner, University of Oregon, Eugene, OR, and approved August 6, 2013 (received for review April 29, 2013)
Significance
Early adversity has profound and lasting effects on neurodevelopment and emotional behavior. Under typical environmental conditions, prefrontal cortex connections with the amygdala are immature during childhood and become adult-like during adolescence. Rodent models show that maternal deprivation accelerates this development as an ontogenetic adaptation to adversity. Here, we demonstrate that, as in the rodent, children who experienced early maternal deprivation exhibit early emergence of mature amygdala–prefrontal connectivity. Evidence suggests that the adult-like neural phenotype, which is mediated by cortisol levels, confers some degree of enhanced emotion regulation, as maternally deprived youths with adult-like phenotypes are less anxious than their counterparts with immature phenotypes. Accelerated amygdala–prefrontal development may serve as an ontogenetic adaptation in the human in response to early adversity.
Abstract
Under typical conditions, medial prefrontal cortex (mPFC) connections with the amygdala are immature during childhood and become adult-like during adolescence. Rodent models show that maternal deprivation accelerates this development, prompting examination of human amygdala–mPFC phenotypes following maternal deprivation. Previously institutionalized youths, who experienced early maternal deprivation, exhibited atypical amygdala–mPFC connectivity. Specifically, unlike the immature connectivity (positive amygdala–mPFC coupling) of comparison children, children with a history of early adversity evidenced mature connectivity (negative amygdala–mPFC coupling) and thus, resembled the adolescent phenotype. This connectivity pattern was mediated by the hormone cortisol, suggesting that stress-induced modifications of the hypothalamic–pituitary–adrenal axis shape amygdala–mPFC circuitry. Despite being age-atypical, negative amygdala–mPFC coupling conferred some degree of reduced anxiety, although anxiety was still significantly higher in the previously institutionalized group. These findings suggest that accelerated amygdala–mPFC development is an ontogenetic adaptation in response to early adversity.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: nimtottenham{at}ucla.edu.
Author contributions: D.G.G., L.J.G.-D., J.F., B.G., K.L.H., E.H.T., T.A.H., S.Y.B., and N.T. designed research; D.G.G., L.J.G.-D., J.F., B.G., K.L.H., E.H.T., and N.T. performed research; D.G.G., T.A.H., and N.T. analyzed data; and D.G.G., T.A.H., S.Y.B., and N.T. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1307893110/-/DCSupplemental.
Adversity accelerates amygdala–PFC development
Article Classifications
- Social Sciences
- Psychological and Cognitive Sciences
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