Adiposity in Adolescence has Detrimental Effects on Developing Brain Structures and Organization, Communication, and Controllability of Resting-State Networks

Abstract

Adiposity in adolescence can have detrimental effects on neural maturation, and is associated with incompletely understood alterations in brain structures and circuits. To address this important knowledge gap, N=3,341 youth from the Adolescent Brain Cognitive Development (ABCD) two-year follow-up cohort (median(IQR) age=12.0(1.1) years; 51.0% females), with structural MRI and resting-state fMRI were studied. Topological properties reflecting network strength, resilience, efficiency and modularity, information transfer, regional feedback costs associated with controllability of network dynamics, and morphometric characteristics were examined as a function of body mass index (BMI), body roundness index (BRI), overweight, obesity, and persistent excess BMI (across assessments). Youth who slept less, spent more time on electronic devices, were Hispanic and/or from lower-income families had higher BMI/BRI ({beta}=0.07-4.95, 95%CI=[0.03,7.05]), and higher odds of overweight or obesity (aOR=1.01-1.72, 95%CI=[1.01,2.28]). Higher BMI/BRI, overweight, obesity and/or persistent excess BMI were associated with weaker and less resilient networks supporting decision-making, control, emotional regulation, reward processing and social function ({beta}=-0.11 to -0.01, CI=[-0.16, -0.01]), and more topologically fragile thalamus and basal ganglia ({beta}=0.05-0.10, CI=[0.01,0.14], p<0.03). They were also associated with lower control costs in cognitive and topological hubs (including the precuneus and prefrontal regions) that play central roles in regulating brain dynamics, aberrant information transfer in limbic, frontoparietal, salience, somatomotor and cerebellar regions, and lower thickness and/or volume of distributed (including prefrontal) regions, and functional hubs ({beta}=-0.14 to -0.02, CI=[-0.18,-0.01]). Thus, adiposity in adolescence is associated with widespread structural and alterations of brain networks supporting developing cognitive processes, and fundamental mechanisms that control these networks dynamics.