Adolescent development of multiscale structural wiring and functional interactions in the human connectome

Author:

Park Bo-yong123ORCID,Paquola Casey14,Bethlehem Richard A. I.56ORCID,Benkarim Oualid1ORCID,Mišić Bratislav1ORCID,Smallwood Jonathan7,Bullmore Edward T.6ORCID,Bernhardt Boris C.1ORCID,Bullmore Edward,Dolan Raymond,Goodyer Ian,Fonagy Peter,Jones Peter,Moutoussis Michael,Hauser Tobias,Neufeld Sharon,Romero-Garcia Rafael,St Clair Michelle,Vértes Petra,Whitaker Kirstie,Inkster Becky,Prabhu Gita,Ooi Cinly,Toseeb Umar,Widmer Barry,Bhatti Junaid,Villis Laura,Alrumaithi Ayesha,Birt Sarah,Bowler Aislinn,Cleridou Kalia,Dadabhoy Hina,Davies Emma,Firkins Ashlyn,Granville Sian,Harding Elizabeth,Hopkins Alexandra,Isaacs Daniel,King Janchai,Kokorikou Danae,Maurice Christina,McIntosh Cleo,Memarzia Jessica,Mills Harriet,O’Donnell Ciara,Pantaleone Sara,Scott Jenny,Kiddle Beatrice,Polek Ela,Fearon Pasco,Suckling John,van Harmelen Anne-Laura,Kievit Rogier,Chamberlain Sam,

Affiliation:

1. McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, H3A 2B4, Canada

2. Department of Data Science, Inha University, Incheon, 22212, Republic of Korea

3. Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon, 16419, Republic of Korea

4. Institute of Neuroscience and Medicine, Forschungszentrum Jülich, Jülich, 52428, Germany

5. Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, United Kingdom

6. Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, United Kingdom

7. Department of Psychology, Queen’s University, Kingston, ON, K7L 3N6, Canada

Abstract

Adolescence is a time of profound changes in the physical wiring and function of the brain. Here, we analyzed structural and functional brain network development in an accelerated longitudinal cohort spanning 14 to 25 y ( n = 199). Core to our work was an advanced in vivo model of cortical wiring incorporating MRI features of corticocortical proximity, microstructural similarity, and white matter tractography. Longitudinal analyses assessing age-related changes in cortical wiring identified a continued differentiation of multiple corticocortical structural networks in youth. We then assessed structure–function coupling using resting-state functional MRI measures in the same participants both via cross-sectional analysis at baseline and by studying longitudinal change between baseline and follow-up scans. At baseline, regions with more similar structural wiring were more likely to be functionally coupled. Moreover, correlating longitudinal structural wiring changes with longitudinal functional connectivity reconfigurations, we found that increased structural differentiation, particularly between sensory/unimodal and default mode networks, was reflected by reduced functional interactions. These findings provide insights into adolescent development of human brain structure and function, illustrating how structural wiring interacts with the maturation of macroscale functional hierarchies.

Funder

National Research Foundation of Korea

Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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