Background

Early adversity is commonly associated with alterations of amygdala circuitry and increased anxiety. While many theoretical and clinical accounts of early adversity suggest that it increases vigilance to threatening stimuli, the present study tested whether heightened anxiety and amygdala reactivity associated with early adversity enhanced goal-directed attention for threatening stimuli. Showing this association would provide support that these adversity-induced alterations are developmental adaptations of the individual.

Methods

34 children and adolescents who experienced early adversity in the form of previous institutionalization (PI) (26 female, mean age=13.49 years) and a comparison group of 33 children and adolescents who were reared by their biological parents since birth (16 female, mean age=13.40 years) underwent fMRI scanning while completing a visual search task that involved quickly locating a negative (fearful face) or positive target (happy face) in an array of neutral distractor stimuli (neutral faces).

Results

Across both groups, individual differences in vigilant behavior were positively associated with amygdala responses for negative versus positive stimuli. However, a moderation analysis revealed that the degree to which amygdala responses were greater for negative versus positive stimuli was associated with greater anxiety symptomology for PI youth, but not comparison youth.

Conclusions

Together, these findings suggest that institutional care strengthens linkages between amygdala reactivity and anxiety, perhaps serving to enhance goal-directed attention. The findings are discussed as both adaptations as well as risk to the individual.

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.