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

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.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-08-09
DOI
https://doi.org/10.1073/pnas.2314074121
Citations
8
Primary Topic
Functional Brain Connectivity Studies
Type
article
Field-Weighted Citation Impact
2.74

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article

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

Beatrice Kiddle, Anne‐Laura van Harmelen, Richard A. I. Bethlehem, Sharon Neufeld et al.
8 citations
Proceedings of the National Academy of Sciences
Functional Brain Connectivity Studies
2.74
article

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

Beatrice Kiddle, Anne‐Laura van Harmelen, Richard A. I. Bethlehem, Sharon Neufeld, Becky Inkster, Sian Granville, Aaron Alexander‐Bloch, Petra E. Vértes, Peter Fonagy, Rafael Romero-García, Ayesha Alrumaithi, John Suckling, Raymond J. Dolan, Sara Pantaleone, Daniel Isaacs, Aislinn Bowler, Simon Richard White, Cinly Ooi, Emma Davies, Harriet L. Mills, Danae Kokorikou, Pasco Fearon, Gita Prabhu, Theodore Daniel Satterthwaite, Alexandra Hopkins, Edward Thomas Bullmore, Tobias U. Hauser, Jenny Scott, Christina Maurice, Sam Chamberlain, Ashlyn Firkins, Kalia Cleridou, Hina Dadabhoy, Sarah Birt, Jakob Seidlitz, Rogier Kievit, Matthew Cieslak, Kirstie Whitaker, Kahini Mehta, Ela Polek, Elizabeth Harding, Ciara O’Donnell, František Váša, Laura Villis, Jessica Memarzia, Cleo McIntosh, Peter Brian Jones, Janchai King, Umar Toseeb, Michelle St Clair, Lena Dorfschmidt, Manfred G. Kitzbichler, Barry Widmer, Michael Moutoussis, Ian Goodyer, Junaid Bhatti
article en
8 citations

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.

Proceedings of the National Academy of SciencesVol. 121(33)
National Health Service (GB), Children's Hospital of Philadelphia (US), King's College London (GB), University of Cambridge (GB), Cambridge University Hospitals NHS Foundation Trust (GB), Instituto de Biomedicina de Sevilla (ES), Lifespan (US), Hospital Universitario Virgen del Rocío (ES), Universidad de Sevilla (ES), University of Pennsylvania (US)
Gates Cambridge Trust
Good health and well-being
Openalex Percentile: Top 10%
Functional Brain Connectivity Studies
2.74
DOIOpen Access PDFOpenAlex
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