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

Váša, František, Romero-Garcia, Rafael, Kitzbichler, Manfred G., Seidlitz, Jakob, Whitaker, Kirstie J., Vaghi, Matilde M. ORCID:, Kundu, Prantik, Patel, Ameera X., Fonagy, Peter, Dolan, Raymond J., Jones, Peter B., Goodyer, Ian M., Vértes, Petra E. and Bullmore, Edward T. and NSPN Consortium (2020) Conservative and disruptive modes of adolescent change in human brain functional connectivity. Proceedings of the National Academy of Sciences of the United States of America, 117 (6). pp. 3248-3253. ISSN 0027-8424

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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, FC14) and adolescent change in FC (ΔFC14−26), 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.

Item Type: Article
Additional Information: ACKNOWLEDGMENTS. This study was supported by the Neuroscience in Psychiatry Network Wellcome Trust Strategic Award 095844/Z/11/Z (to the University of Cambridge and University College London). Additional support was provided by the National Institute for Health Research (NIHR) Cambridge Biomedical Research Center. F.V. was supported by the Gates Cambridge Trust; additional support was provided by the NIHR Biomedical Research Centre at South London and Maudsley National Health Service (NHS) Foundation Trust, and King’s College London. K.J.W. and P.E.V. are Fellows of the Alan Turing Institute funded by Engineering and Physical Sciences Research Council (EPSRC) Grant EP/N510129/1. P.F. is an NIHR Senior Investigator (Grant NF-SI-0514-10157) and was in part supported by the NIHR Collaboration for Leadership in Applied Health Research and Care North Thames at Barts Health NHS Trust. P.E.V. was supported by Medical Research Council (MRC) Grant MR/K020706/1 and is a Fellow of MQ: Transforming Mental Health (Grant MQF17/24). E.T.B. is an NIHR Senior Investigator. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, or the Department of Health and Social Care. We thank Lena Dorfschmidt for corrections of analysis code.
Uncontrolled Keywords: allen human brain atlas,connectome,head movement,mri,neurodevelopment,general,sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/1000
Faculty \ School: Faculty of Social Sciences > School of Psychology
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Depositing User: LivePure Connector
Date Deposited: 04 Oct 2022 13:05
Last Modified: 03 Nov 2022 16:38
DOI: 10.1073/pnas.1906144117

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