Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation

TLDR

Early adversity profoundly affects neurodevelopment, and while prefrontal–amygdala connections normally mature during adolescence, rodent studies show maternal deprivation accelerates this process as an adaptive response. We found that children who experienced early maternal deprivation show premature maturation of amygdala–prefrontal connectivity, a cortisol‑mediated adult‑like phenotype associated with reduced anxiety, suggesting accelerated development as an adaptive response to early adversity.

Abstract

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.