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

2021; eLife Sciences Publications Ltd; Volume: 10; Linguagem: Inglês

10.7554/elife.64694

2050-084X

Bo‐yong Park, Richard A. I. Bethlehem, Casey Paquola, Sara Larivière, Raúl Rodríguez‐Cruces, Reinder Vos de Wael, 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 Jane 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 Harmelen, Rogier Kievit, Sam Chamberlain, Edward T. Bullmore, Boris C. Bernhardt,

Advanced Neuroimaging Techniques and Applications

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.