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

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 adolesce...

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Autores principales: Váša, František, Romero-Garcia, Rafael, Kitzbichler, Manfred G., Seidlitz, Jakob, Whitaker, Kirstie J., Vaghi, Matilde M., Kundu, Prantik, Patel, Ameera X., Fonagy, Peter, Dolan, Raymond J., Jones, Peter B., Goodyer, Ian M., Vértes, Petra E., Bullmore, Edward T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022153/
https://www.ncbi.nlm.nih.gov/pubmed/31992644
http://dx.doi.org/10.1073/pnas.1906144117
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author Váša, František
Romero-Garcia, Rafael
Kitzbichler, Manfred G.
Seidlitz, Jakob
Whitaker, Kirstie J.
Vaghi, Matilde M.
Kundu, Prantik
Patel, Ameera X.
Fonagy, Peter
Dolan, Raymond J.
Jones, Peter B.
Goodyer, Ian M.
Vértes, Petra E.
Bullmore, Edward T.
author_facet Váša, František
Romero-Garcia, Rafael
Kitzbichler, Manfred G.
Seidlitz, Jakob
Whitaker, Kirstie J.
Vaghi, Matilde M.
Kundu, Prantik
Patel, Ameera X.
Fonagy, Peter
Dolan, Raymond J.
Jones, Peter B.
Goodyer, Ian M.
Vértes, Petra E.
Bullmore, Edward T.
author_sort Váša, František
collection PubMed
description 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.
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spelling pubmed-70221532020-02-21 Conservative and disruptive modes of adolescent change in human brain functional connectivity Váša, František Romero-Garcia, Rafael Kitzbichler, Manfred G. Seidlitz, Jakob Whitaker, Kirstie J. Vaghi, Matilde M. Kundu, Prantik Patel, Ameera X. Fonagy, Peter Dolan, Raymond J. Jones, Peter B. Goodyer, Ian M. Vértes, Petra E. Bullmore, Edward T. Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2020-02-11 2020-01-28 /pmc/articles/PMC7022153/ /pubmed/31992644 http://dx.doi.org/10.1073/pnas.1906144117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Váša, František
Romero-Garcia, Rafael
Kitzbichler, Manfred G.
Seidlitz, Jakob
Whitaker, Kirstie J.
Vaghi, Matilde M.
Kundu, Prantik
Patel, Ameera X.
Fonagy, Peter
Dolan, Raymond J.
Jones, Peter B.
Goodyer, Ian M.
Vértes, Petra E.
Bullmore, Edward T.
Conservative and disruptive modes of adolescent change in human brain functional connectivity
title Conservative and disruptive modes of adolescent change in human brain functional connectivity
title_full Conservative and disruptive modes of adolescent change in human brain functional connectivity
title_fullStr Conservative and disruptive modes of adolescent change in human brain functional connectivity
title_full_unstemmed Conservative and disruptive modes of adolescent change in human brain functional connectivity
title_short Conservative and disruptive modes of adolescent change in human brain functional connectivity
title_sort conservative and disruptive modes of adolescent change in human brain functional connectivity
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022153/
https://www.ncbi.nlm.nih.gov/pubmed/31992644
http://dx.doi.org/10.1073/pnas.1906144117
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