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Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence.

ABSTRACT: Early life stress (ELS) and function of the hypothalamic-pituitary-adrenal axis predict later psychopathology. Animal studies and cross-sectional human studies suggest that this process might operate through amygdala-ventromedial prefrontal cortex (vmPFC) circuitry implicated in the regulation of emotion. Here we prospectively investigated the roles of ELS and childhood basal cortisol amounts in the development of adolescent resting-state functional connectivity (rs-FC), assessed by functional connectivity magnetic resonance imaging (fcMRI), in the amygdala-PFC circuit. In females only, greater ELS predicted increased childhood cortisol levels, which predicted decreased amygdala-vmPFC rs-FC 14 years later. For females, adolescent amygdala-vmPFC functional connectivity was inversely correlated with concurrent anxiety symptoms but positively associated with depressive symptoms, suggesting differing pathways from childhood cortisol levels function through adolescent amygdala-vmPFC functional connectivity to anxiety and depression. These data highlight that, for females, the effects of ELS and early HPA-axis function may be detected much later in the intrinsic processing of emotion-related brain circuits.

SUBMITTER: Burghy CA

PROVIDER: S-EPMC3509229 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence.

Burghy Cory A CA Stodola Diane E DE Ruttle Paula L PL Molloy Erin K EK Armstrong Jeffrey M JM Oler Jonathan A JA Fox Michelle E ME Hayes Andrea S AS Kalin Ned H NH Essex Marilyn J MJ Davidson Richard J RJ Birn Rasmus M RM

Nature neuroscience 20121111 12

Early life stress (ELS) and function of the hypothalamic-pituitary-adrenal axis predict later psychopathology. Animal studies and cross-sectional human studies suggest that this process might operate through amygdala-ventromedial prefrontal cortex (vmPFC) circuitry implicated in the regulation of emotion. Here we prospectively investigated the roles of ELS and childhood basal cortisol amounts in the development of adolescent resting-state functional connectivity (rs-FC), assessed by functional c ...[more]

PMID: 23143517

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Project description:BACKGROUND:Much research has focused on the deleterious neurobiological effects of childhood adversity that may underlie internalizing disorders. While most youth show emotional adaptation following adversity, the corresponding neural mechanisms remain poorly understood. METHODS:In this longitudinal community study, we examined the associations among childhood family adversity, adolescent internalizing symptoms, and their interaction on regional brain activation and amygdala/hippocampus functional connectivity during emotion processing in 132 adolescents. RESULTS:Consistent with prior work, childhood adversity predicted heightened amygdala reactivity to negative, but not positive, images in adolescence. However, amygdala reactivity was not related to internalizing symptoms. Furthermore, childhood adversity predicted increased fronto-amygdala connectivity to negative, but not positive, images, yet only in lower internalizing adolescents. Childhood adversity also predicted increased fronto-hippocampal connectivity to negative images, but was not moderated by internalizing. These findings were unrelated to adolescence adversity or externalizing symptoms, suggesting specificity to childhood adversity and adolescent internalizing. CONCLUSIONS:Together, these findings suggest that adaptation to childhood adversity is associated with augmentation of fronto-subcortical circuits specifically for negative emotional stimuli. Conversely, insufficient enhancement of fronto-amygdala connectivity, with increasing amygdala reactivity, may represent a neural signature of vulnerability for internalizing by late adolescence. These findings implicate early childhood as a critical period in determining the brain's adaptation to adversity, and suggest that even normative adverse experiences can have significant impact on neurodevelopment and functioning. These results offer potential neural mechanisms of adaptation and vulnerability which could be used in the prediction of risk for psychopathology following childhood adversity.

Project description:Ecological stress during adolescent development may increase the sensitivity to negative emotional processes that can contribute to the onset and progression of internalizing behaviors during preadolescence. Although a small number of studies have considered the link among the relations between ecological stress, amygdala reactivity, and internalizing symptoms in childhood and adolescence, these studies have largely been small, cross-sectional, and often do not consider unique roles of parenting or sex. In the current study, we evaluated the interrelations between ecological stress, amygdala reactivity, subsequent internalizing symptoms, and the moderating roles of parenting and sex among 9- and 10-year-old preadolescents from the Adolescent Brain Cognitive Development (ABCD) Study ®. A subset of participants who met a priori quality control criteria for bilateral amygdala activation during the EN-back faces versus places contrast (N = 7,385; Mean Age = 120 months, SD = 7.52; 49.5% Female) were included in the study. A confirmatory factor analysis was performed to create a latent variable of ecological stress, and multiple structural equation models were tested to evaluate the association among baseline ecological stress and internalizing symptoms one year later, the mediating role of amygdala reactivity, and moderating effects of parental acceptance and sex. The results revealed a significant association between ecological stress and subsequent internalizing symptoms, which was greater in males than females. There was no association between amygdala reactivity during the Faces versus Places contrast and ecological stress or subsequent internalizing symptoms, and no mediating role of amygdala or moderating effect of parental acceptance on the association between ecological stress and internalizing symptoms. An alternative mediation model was tested which revealed that there was a small mediating effect of parental acceptance on the association between ecological stress and internalizing symptoms, demonstrating lower internalizing symptoms among preadolescents one year later. Given the lack of association in brain function, ecological stress and internalizing symptoms in preadolescents in this registered report, effects from comparable small studies should be reconsidered in larger samples.

Dataset Information

Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence.

Publications

Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence.

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