Conservative and disruptive modes of adolescent change in human brain functional connectivity
František Váša, Rafael Romero-García, Manfred G. Kitzbichler, Jakob Seidlitz, Kirstie Whitaker, Matilde M. Vaghi, Prantik Kundu, Ameera X. Patel, Peter Fonagy, Raymond J. Dolan, Peter B. Jones, Ian M. Goodyer, Petra E. Vértes, Edward T. Bullmore, Edward T. Bullmore, Raymond J. Dolan, Ian Goodyer, Peter Fonagy, Peter B. Jones, Michael Moutoussis, Tobias U. Hauser, Sharon Neufeld, Rafael Romero-García, Michelle St Clair, Petra E. Vértes, Kirstie Whitaker, Becky Inkster, Gita Prabhu, Cinly Ooi, Umar Toseeb, Barry Widmer, Junaid Bhatti, Laura Villis, Ayesha Alrumaithi, Sarah Birt, Aislinn Bowler, Kalia Cleridou, Hina Dadabhoy, Emma Davies, Ashlyn Firkins, Sian Granville, Elizabeth Harding, Alexandra Hopkins, Daniel Isaacs, Janchai King, Danae Kokorikou, Christina Maurice, Cleo McIntosh, Jessica Memarzia, Harriet L. Mills, Ciara O’Donnell, Sara Pantaleone, Jenny Scott, Pasco Fearon, John Suckling, Anne‐Laura van Harmelen, Rogier Kievit
Abstract
Adolescent changes in human brain function are not entirely understood. Here, we used multiecho functional MRI (fMRI) to measure developmental change in functional connectivity (FC) of resting-state oscillations between pairs of 330 cortical regions and 16 subcortical regions in 298 healthy adolescents scanned 520 times. Participants were aged 14 to 26 y and were scanned on 1 to 3 occasions at least 6 mo apart. We found 2 distinct modes of age-related change in FC: "conservative" and "disruptive." Conservative development was characteristic of primary cortex, which was strongly connected at 14 y and became even more connected in the period from 14 to 26 y. Disruptive development was characteristic of association cortex and subcortical regions, where connectivity was remodeled: connections that were weak at 14 y became stronger during adolescence, and connections that were strong at 14 y became weaker. These modes of development were quantified using the maturational index (MI), estimated as Spearman's correlation between edgewise baseline FC (at 14 y, [Formula: see text]) and adolescent change in FC ([Formula: see text]), at each region. Disruptive systems (with negative MI) were activated by social cognition and autobiographical memory tasks in prior fMRI data and significantly colocated with prior maps of aerobic glycolysis (AG), AG-related gene expression, postnatal cortical surface expansion, and adolescent shrinkage of cortical thickness. The presence of these 2 modes of development was robust to numerous sensitivity analyses. We conclude that human brain organization is disrupted during adolescence by remodeling of FC between association cortical and subcortical areas.