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Proc Natl Acad Sci U S A. 2020 Jan 28. pii: 201906144. doi: 10.1073/pnas.1906144117. [Epub ahead of print]

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

Author information

1
Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, United Kingdom; fdv247@gmail.com.
2
Department of Neuroimaging, Institute of Psychiatry, Psychology and Neurosciences, King's College London, London SE5 8AF, United Kingdom.
3
Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, United Kingdom.
4
Developmental Neurogenomics Unit, National Institute of Mental Health, Bethesda, MD 20892.
5
The Alan Turing Institute, London NW1 2DB, United Kingdom.
6
Wellcome Trust Centre for Neuroimaging, University College London Institute of Neurology, University College London, London WC1N 3BG, United Kingdom.
7
Research Department of Clinical, Educational and Health Psychology, University College London, London WC1E 6BT, United Kingdom.
8
Brain Imaging Center, Icahn School of Medicine at Mount Sinai, New York, NY 10029.
9
Cambridgeshire and Peterborough National Health Service (NHS) Foundation Trust, Huntingdon PE29 3RJ, United Kingdom.
10
School of Mathematical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom.

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, [Formula: see text]) and adolescent change in FC ([Formula: see text]), 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.

KEYWORDS:

Allen Human Brain Atlas; MRI; connectome; head movement; neurodevelopment

PMID:
31992644
DOI:
10.1073/pnas.1906144117
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Conflict of interest statement

The authors declare no competing interest.

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