An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

• DOI: 10.7554/elife.64694
• Publication Date: 2021-03-31T12:00:46Z
• Authors: Bo-yong Park; Richard AI Bethlehem; Casey Paquola; Sara Larivière; Raul Rodríguez-Cr...; Reinder Vos de Wael; ; Edward Bullmore; Raymond Dolan; Ian Goodyer; Peter Fonagy; Peter Jones; Michael Moutoussis; Tobias Hauser; Sharon Neufeld; Rafael Romero-Garcia; Michelle St Clair; Petra 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 Mills; Ciara O’Donnell; Sara Pantaleone; Jenny Scott; Beatrice Kiddle; Ela Polek; Pasco Fearon; John Suckling; Anne-Laura van Ha...; Rogier Kievit; Sam Chamberlain; Edward T Bullmore; Boris C Bernhardt
• Keywords: Adult; Male; 0301 basic medicine; Adolescent; longitudinal; QH301-705.5; multi-scale; Science; Neurogenesis; Models, Neurological; Nerve Tissue Proteins; neuroscience; Young Adult; 03 medical and health sciences; Cognition; Neural Pathways; Connectome; Humans; human; Longitudinal Studies; Biology (General); neuroimaging; neurodevelopment; Gene Expression Profiling; Q; connectome; R; Age Factors; Brain; Gene Expression Regulation, Developmental; Adolescent Development; Magnetic Resonance Imaging; 3. Good health; Adolescent Behavior; info:eu-repo/classification/ddc/600; Medicine; Female; adolescence; Transcriptome; Research Article; Neuroscience; Human

Adolescence is a critical time for the continued maturation of brain networks. Here, we assessed structural connectome development in a large longitudinal sample ranging from childhood to young adulthood. By projecting high-dimensional connectomes into compact manifold spaces, we identified a marked expansion of structural connectomes, with strongest effects in transmodal regions during adolescence. Findings reflected increased within-module connectivity together with increased segregation, indicating increasing differentiation of higher-order association networks from the rest of the brain. Projection of subcortico-cortical connectivity patterns into these manifolds showed parallel alterations in pathways centered on the caudate and thalamus. Connectome findings were contextualized via spatial transcriptome association analysis, highlighting genes enriched in cortex, thalamus, and striatum. Statistical learning of cortical and subcortical manifold features at baseline and their maturational change predicted measures of intelligence at follow-up. Our findings demonstrate that connectome manifold learning can bridge the conceptual and empirical gaps between macroscale network reconfigurations, microscale processes, and cognitive outcomes in adolescent development.