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Human adolescent brain similarity development is different for paralimbic versus neocortical zones.

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Peer-reviewed

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Abstract

Adolescent development of human brain structural and functional networks is increasingly recognized as fundamental to emergence of typical and atypical adult cognitive and emotional proodal magnetic resonance imaging (MRI) data collected from N [Formula: see text] 300 healthy adolescents (51%; female; 14 to 26 y) each scanned repeatedly in an accelerated longitudinal design, to provide an analyzable dataset of 469 structural scans and 448 functional MRI scans. We estimated the morphometric similarity between each possible pair of 358 cortical areas on a feature vector comprising six macro- and microstructural MRI metrics, resulting in a morphometric similarity network (MSN) for each scan. Over the course of adolescence, we found that morphometric similarity increased in paralimbic cortical areas, e.g., insula and cingulate cortex, but generally decreased in neocortical areas, and these results were replicated in an independent developmental MRI cohort (N [Formula: see text] 304). Increasing hubness of paralimbic nodes in MSNs was associated with increased strength of coupling between their morphometric similarity and functional connectivity. Decreasing hubness of neocortical nodes in MSNs was associated with reduced strength of structure-function coupling and increasingly diverse functional connections in the corresponding fMRI networks. Neocortical areas became more structurally differentiated and more functionally integrative in a metabolically expensive process linked to cortical thinning and myelination, whereas paralimbic areas specialized for affective and interoceptive functions became less differentiated, as hypothetically predicted by a developmental transition from periallocortical to proisocortical organization of the cortex. Cytoarchitectonically distinct zones of the human cortex undergo distinct neurodevelopmental programs during typical adolescence.

Description

Journal Title

Proc Natl Acad Sci U S A

Conference Name

Journal ISSN

0027-8424
1091-6490

Volume Title

Publisher

Proceedings of the National Academy of Sciences

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Except where otherwised noted, this item's license is described as Attribution 4.0 International
Sponsorship
Wellcome Trust (095844/Z/11/Z)
MQ: Transforming Mental Health (MQ17-24 Vertes)
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. L.D. was supported by the Gates Cambridge Trust. R.A.I.B. was supported by the Autism Research Trust and the Centre for Integrative Neuroscience Discovery. P.E.V. was supported by an MQ: Transforming Mental Health Fellowship MQF17\_24. E.T.B. is an NIHR Senior Investigator. R.R.-G. was funded by the EMERGIA Junta de Andaluc\'{i}a program (EMERGIA20\_00139) and the Spanish Ministry of Science and Innovation (PID2021-122853OA-I00). 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.

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