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Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence

The transition from childhood to adolescence is marked by pronounced shifts in brain structure and function that coincide with the development of physical, cognitive, and social abilities. Prior work in adult populations has characterized the topographical organization of the cortex, revealing macro...

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Autores principales: Dong, Hao-Ming, Margulies, Daniel S., Zuo, Xi-Nian, Holmes, Avram J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8285909/
https://www.ncbi.nlm.nih.gov/pubmed/34260385
http://dx.doi.org/10.1073/pnas.2024448118
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author Dong, Hao-Ming
Margulies, Daniel S.
Zuo, Xi-Nian
Holmes, Avram J.
author_facet Dong, Hao-Ming
Margulies, Daniel S.
Zuo, Xi-Nian
Holmes, Avram J.
author_sort Dong, Hao-Ming
collection PubMed
description The transition from childhood to adolescence is marked by pronounced shifts in brain structure and function that coincide with the development of physical, cognitive, and social abilities. Prior work in adult populations has characterized the topographical organization of the cortex, revealing macroscale functional gradients that extend from unimodal (somatosensory/motor and visual) regions through the cortical association areas that underpin complex cognition in humans. However, the presence of these core functional gradients across development as well as their maturational course have yet to be established. Here, leveraging 378 resting-state functional MRI scans from 190 healthy individuals aged 6 to 17 y old, we demonstrate that the transition from childhood to adolescence is reflected in the gradual maturation of gradient patterns across the cortical sheet. In children, the overarching organizational gradient is anchored within the unimodal cortex, between somatosensory/motor and visual territories. Conversely, in adolescence, the principal gradient of connectivity transitions into an adult-like spatial framework, with the default network at the opposite end of a spectrum from primary sensory and motor regions. The observed gradient transitions are gradually refined with age, reaching a sharp inflection point in 13 and 14 y olds. Functional maturation was nonuniformly distributed across cortical networks. Unimodal networks reached their mature positions early in development, while association regions, in particular the medial prefrontal cortex, reached a later peak during adolescence. These data reveal age-dependent changes in the macroscale organization of the cortex and suggest the scheduled maturation of functional gradient patterns may be critically important for understanding how cognitive and behavioral capabilities are refined across development.
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spelling pubmed-82859092021-07-26 Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence Dong, Hao-Ming Margulies, Daniel S. Zuo, Xi-Nian Holmes, Avram J. Proc Natl Acad Sci U S A Social Sciences The transition from childhood to adolescence is marked by pronounced shifts in brain structure and function that coincide with the development of physical, cognitive, and social abilities. Prior work in adult populations has characterized the topographical organization of the cortex, revealing macroscale functional gradients that extend from unimodal (somatosensory/motor and visual) regions through the cortical association areas that underpin complex cognition in humans. However, the presence of these core functional gradients across development as well as their maturational course have yet to be established. Here, leveraging 378 resting-state functional MRI scans from 190 healthy individuals aged 6 to 17 y old, we demonstrate that the transition from childhood to adolescence is reflected in the gradual maturation of gradient patterns across the cortical sheet. In children, the overarching organizational gradient is anchored within the unimodal cortex, between somatosensory/motor and visual territories. Conversely, in adolescence, the principal gradient of connectivity transitions into an adult-like spatial framework, with the default network at the opposite end of a spectrum from primary sensory and motor regions. The observed gradient transitions are gradually refined with age, reaching a sharp inflection point in 13 and 14 y olds. Functional maturation was nonuniformly distributed across cortical networks. Unimodal networks reached their mature positions early in development, while association regions, in particular the medial prefrontal cortex, reached a later peak during adolescence. These data reveal age-dependent changes in the macroscale organization of the cortex and suggest the scheduled maturation of functional gradient patterns may be critically important for understanding how cognitive and behavioral capabilities are refined across development. National Academy of Sciences 2021-07-13 2021-07-06 /pmc/articles/PMC8285909/ /pubmed/34260385 http://dx.doi.org/10.1073/pnas.2024448118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Social Sciences
Dong, Hao-Ming
Margulies, Daniel S.
Zuo, Xi-Nian
Holmes, Avram J.
Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
title Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
title_full Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
title_fullStr Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
title_full_unstemmed Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
title_short Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
title_sort shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence
topic Social Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8285909/
https://www.ncbi.nlm.nih.gov/pubmed/34260385
http://dx.doi.org/10.1073/pnas.2024448118
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