Pubertal development mediates the association between family environment and brain structure and function in childhood

Abstract

Psychosocial acceleration theory suggests that pubertal maturation is accelerated in response to adversity. In addition, suboptimal caregiving accelerates development of the amygdala–medial prefrontal cortex circuit. These findings may be related. Here, we assess whether associations between family environment and measures of the amygdala–medial prefrontal cortex circuit are mediated by pubertal development in more than 2000 9- and 10-year-old children from the Adolescent Brain Cognitive Development Study (http://dx.doi.org/10.15154/1412097). Using structural equation modeling, demographic, child-reported, and parent-reported data on family dynamics were compiled into a higher level family environment latent variable. Magnetic resonance imaging preprocessing and compilations were performed by the Adolescent Brain Cognitive Development Study's data analysis core. Anterior cingulate cortex (ACC) thickness, area, white matter fractional anisotropy, amygdala volume, and cingulo-opercular network–amygdala resting-state functional connectivity were assessed. For ACC cortical thickness and ACC fractional anisotropy, significant indirect effects indicated that a stressful family environment relates to more advanced pubertal stage and more mature brain structure. For cingulo-opercular network–amygdala functional connectivity, results indicated a trend in the expected direction. For ACC area, evidence for quadratic mediation by pubertal stage was found. Sex-stratified analyses suggest stronger results for girls. Despite small effect sizes, structural measures of circuits important for emotional behavior are associated with family environment and show initial evidence of accelerated pubertal development.

Associations among negative life events, changes in cortico-limbic connectivity, and psychopathology in the ABCD Study

“…Thus, adolescents in this sample who had experienced more negative life events may have adapted to more stressful contexts via accelerated maturation in CO-amygdala-hippocampal connections. Consistent with this finding, a recent investigation with ABCD data found that accelerated pubertal maturation mediated the association between stressful family environments and CO network-amygdala rsFC ( Thijssen et al, 2020a , Thijssen et al, 2020b ). The current longitudinal findings also extend prior cross-sectional evidence of stress acceleration in cortico-limbic circuitry ( Gee et al, 2013a , Herzberg et al, 2021 , Miller et al, 2020 , Silvers et al, 2016 , Thijssen et al, 2017 ).…”

“…Theoretical and empirical work across species suggests that exposure to adversity may accelerate these patterns of maturation ( Callaghan and Tottenham, 2016 , Gee et al, 2013a , Herzberg et al, 2021 , Miller et al, 2020 , Silvers et al, 2016 , Thijssen et al, 2017 ). For example, stressful family environments have been linked to accelerated pubertal maturation, which in turn was associated with altered CO-amygdala rsFC, among youth in the Adolescent Brain Cognitive Development Study℠ (ABCD Study®; Thijssen et al, 2020a , Thijssen et al, 2020b ). In this way, accelerated maturation may reflect adaptation to stressful environments and promote short-term resilience to mental health problems.…”

“…At the same time, other work has suggested that adversity exposure is associated with delays or weakening connectivity in certain circuits, and in turn, increased risk for psychopathology (e.g., Rakesh et al, 2021 ). Much of this work has relied on cross-sectional designs (e.g., Gee et al, 2013a ; Herzberg et al, 2021 ; Silvers et al, 2016 ; Thijssen et al, 2020a , Thijssen et al, 2020b ). Additional research, especially with longitudinal neuroimaging, is necessary to disentangle the directions of these associations across development.…”

“…Indeed, the same circuits that are highly sensitive to stress are also implicated in a host of psychopathology outcomes in youth. For example, aberrant patterns of cortico-limbic rsFC may underlie both internalizing ( Rakesh et al, 2021 , VanTieghem and Tottenham, 2018 ) and externalizing ( Rubia, 2011 , Silveira et al, 2021 , Thijssen et al, 2020a , Thijssen et al, 2020b ) symptomatology. More specifically, connectivity between the CO network and subcortical regions has been linked to psychopathology among youth in the ABCD Study.…”

Inter-individual variability in structural brain development from late childhood to young adulthood

“…This secondary focus of the present investigation is motivated by a common inference in the neuroimaging literature that the maturity of a developing individual’s brain size can be assessed by comparing them cross-sectionally to similar-aged peers. For example, children and adolescents with thinner cortex than similar-aged peers are often inferred as more mature, or faster-maturing, in their brain development (e.g., Paulus et al, 2019 ; Tamnes et al, 2018 ; Thijssen et al, 2020 ). In this example, the inference stems from the group-level observation that the cortex of the human brain decreases in thickness across childhood and adolescence, but fails to consider the large amount of variability neurotypically developing children can have in one given brain measure ( Wierenga et al, 2019 ).…”