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

Váša, F. and Romero-Garcia, R. and Kitzbichler, M.G. and Seidlitz, J. and Whitaker, K.J. and Vaghi, Matilde M. and Kundu, P. and Patel, A.X. and Fonagy, P. and Dolan, R.J. and Jones, P.B. and Goodyer, I.M. and Vértes, P.E. and Bullmore, E.T. and Bullmore, E. and Dolan, R. and Goodyer, I. and Fonagy, P. and Jones, P. and Moutoussis, M. and Hauser, T. and Neufeld, S. and Romero-Garcia, R. and St Clair, M. and Vértes, P. and Whitaker, K. and Inkster, B. and Prabhu, G. and Ooi, C. and Toseeb, U. and Widmer, B. and Bhatti, J. and Villis, L. and Alrumaithi, A. and Birt, S. and Bowler, A. and Cleridou, K. and Dadabhoy, H. and Davies, E. and Firkins, A. and Granville, S. and Harding, E. and Hopkins, A. and Isaacs, D. and King, J. and Kokorikou, D. and Maurice, C. and McIntosh, C. and Memarzia, J. and Mills, H. and O’Donnell, C. and Pantaleone, S. and Scott, J. and Fearon, P. and Suckling, J. and van Harmelen, A.-L. and Kievit, R. (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.

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, FC14) and adolescent change in FC ( ), 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.

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