Conservative and disruptive modes of adolescent change in human brain functional connectivity

Abstract

Adolescent changes in human brain function are not entirelyunderstood. Here, we used multiecho functional MRI (fMRI) tomeasure developmental change in functional connectivity (FC) ofresting-state oscillations between pairs of 330 cortical regions and16 subcortical regions in 298 healthy adolescents scanned 520times. Participants were aged 14 to 26 y and were scanned on1 to 3 occasions at least 6 mo apart. We found 2 distinct modes ofage-related change in FC: “conservative” and “disruptive.” Conser-vative development was characteristic of primary cortex, whichwas strongly connected at 14 y and became even more con-nected in the period from 14 to 26 y. Disruptive development wascharacteristic of association cortex and subcortical regions, whereconnectivity was remodeled: connections that were weak at 14 ybecame stronger during adolescence, and connections that werestrong at 14 y became weaker. These modes of development werequantified using the maturational index (MI), estimated as Spear-man’s correlation between edgewise baseline FC (at 14 y, FC14)and adolescent change in FC (∆FC14−26), at each region. Disrup-tive systems (with negative MI) were activated by social cognitionand autobiographical memory tasks in prior fMRI data and sig-nificantly colocated with prior maps of aerobic glycolysis (AG),AG-related gene expression, postnatal cortical surface expansion,and adolescent shrinkage of cortical thickness. The presence ofthese 2 modes of development was robust to numerous sen-sitivity analyses. We conclude that human brain organizationis disrupted during adolescence by remodeling of FC betweenassociation cortical and subcortical areas