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

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 amygdalamPFC 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.fMRI | emotion regulation | stress | neurodevelopment

Mother nurture and the social definition of neurodevelopment

“…Maternal deprivation activates glucocorticoid release, which triggers amygdala maturation. A remarkably similar effect occurs in humans where institutional rearing, an obvious instance of parental deprivation, accelerates functional coupling of the amygdala to the prefrontal cortex (18). This effect is likewise mediated by glucocorticoids, which are inhibited by active maternal care in both rodents and humans (16).…”

Sensitive Periods in Affective Development: Nonlinear Maturation of Fear Learning

“…Although these functional connectivity measures do not directly reflect the non-linear developmental pattern observed in fear extinction and associated synaptic plasticity , they provide an indication of the pronounced maturational changes in the dynamic interaction between these regions. Interestingly, mirroring the early maturation of the fear neurocircuitry induced by maternal separation in the rodent (Callaghan and Richardson, 2011), institutionallyreared children who experienced early maternal deprivation show the more mature pattern of positive vmPFC-amygdala coupling (Gee et al, 2013a). This suggests that, as in rodents, the maturational trajectory of human fear neurocircuitry is also highly sensitive to experiential variation during early development (Tottenham, 2013).…”

Dynamic neural activity during stress signals resilient coping

“…Disrupted VmPFC signaling during stress also predicts alcohol relapse and failed recovery from alcoholism (23). Childhood trauma, cumulative adversity, and a history of mood disorders or posttraumatic stress disorder (PTSD) are each associated with blunted VmPFC activation during emotion or stress exposure, and disrupted VmPFC connectivity with amygdala is suggestive of poor adaptive coping (13,14,16,24,25). On the other hand, it is plausible that brief, sustained stress exposure may provide an approach to assess more automatic neural processes that underlie stress adaptive and resilient coping responses.…”