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Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth

The white matter architecture of the human brain undergoes substantial development throughout childhood and adolescence, allowing for more efficient signaling between brain regions that support executive function. Increasingly, the field understands grey matter development as a spatially and tempora...

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Autores principales: Bagautdinova, Joëlle, Bourque, Josiane, Sydnor, Valerie J, Cieslak, Matt, Alexander-Bloch, Aaron F, Bertolero, Max A, Cook, Phil A, Gur, Raquel C, Gur, Ruben E, Larsen, Bart, Moore, Tyler M, Radhakrishnan, Hamsi, Roalf, David R, Shinohara, Russel T, Tapera, Tinashe M, Zhao, Chenying, Sotiras, Aristeidis, Davatzikos, Christos, Satterthwaite, Theodore D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9934602/
https://www.ncbi.nlm.nih.gov/pubmed/36798354
http://dx.doi.org/10.1101/2023.02.09.527696
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author Bagautdinova, Joëlle
Bourque, Josiane
Sydnor, Valerie J
Cieslak, Matt
Alexander-Bloch, Aaron F
Bertolero, Max A
Cook, Phil A
Gur, Raquel C
Gur, Ruben E
Larsen, Bart
Moore, Tyler M
Radhakrishnan, Hamsi
Roalf, David R
Shinohara, Russel T
Tapera, Tinashe M
Zhao, Chenying
Sotiras, Aristeidis
Davatzikos, Christos
Satterthwaite, Theodore D
author_facet Bagautdinova, Joëlle
Bourque, Josiane
Sydnor, Valerie J
Cieslak, Matt
Alexander-Bloch, Aaron F
Bertolero, Max A
Cook, Phil A
Gur, Raquel C
Gur, Ruben E
Larsen, Bart
Moore, Tyler M
Radhakrishnan, Hamsi
Roalf, David R
Shinohara, Russel T
Tapera, Tinashe M
Zhao, Chenying
Sotiras, Aristeidis
Davatzikos, Christos
Satterthwaite, Theodore D
author_sort Bagautdinova, Joëlle
collection PubMed
description The white matter architecture of the human brain undergoes substantial development throughout childhood and adolescence, allowing for more efficient signaling between brain regions that support executive function. Increasingly, the field understands grey matter development as a spatially and temporally coordinated mechanism that follows hierarchically organized gradients of change. While white matter development also appears asynchronous, previous studies have largely relied on anatomical atlases to characterize white matter tracts, precluding a direct assessment of how white matter structure is spatially and temporally coordinated. Here, we leveraged advances in diffusion modeling and unsupervised machine learning to delineate white matter fiber covariance networks comprised of structurally similar areas of white matter in a cross-sectional sample of 939 youth aged 8–22 years. We then evaluated associations between fiber covariance network structural properties with both age and executive function using generalized additive models. The identified fiber covariance networks aligned with the known architecture of white matter while simultaneously capturing novel spatial patterns of coordinated maturation. Fiber covariance networks showed heterochronous increases in fiber density and cross section that generally followed hierarchically organized temporal patterns of cortical development, with the greatest increases in unimodal sensorimotor networks and the most prolonged increases in superior and anterior transmodal networks. Notably, we found that executive function was associated with structural features of limbic and association networks. Taken together, this study delineates data-driven patterns of white matter network development that support cognition and align with major axes of brain maturation.
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spelling pubmed-99346022023-02-17 Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth Bagautdinova, Joëlle Bourque, Josiane Sydnor, Valerie J Cieslak, Matt Alexander-Bloch, Aaron F Bertolero, Max A Cook, Phil A Gur, Raquel C Gur, Ruben E Larsen, Bart Moore, Tyler M Radhakrishnan, Hamsi Roalf, David R Shinohara, Russel T Tapera, Tinashe M Zhao, Chenying Sotiras, Aristeidis Davatzikos, Christos Satterthwaite, Theodore D bioRxiv Article The white matter architecture of the human brain undergoes substantial development throughout childhood and adolescence, allowing for more efficient signaling between brain regions that support executive function. Increasingly, the field understands grey matter development as a spatially and temporally coordinated mechanism that follows hierarchically organized gradients of change. While white matter development also appears asynchronous, previous studies have largely relied on anatomical atlases to characterize white matter tracts, precluding a direct assessment of how white matter structure is spatially and temporally coordinated. Here, we leveraged advances in diffusion modeling and unsupervised machine learning to delineate white matter fiber covariance networks comprised of structurally similar areas of white matter in a cross-sectional sample of 939 youth aged 8–22 years. We then evaluated associations between fiber covariance network structural properties with both age and executive function using generalized additive models. The identified fiber covariance networks aligned with the known architecture of white matter while simultaneously capturing novel spatial patterns of coordinated maturation. Fiber covariance networks showed heterochronous increases in fiber density and cross section that generally followed hierarchically organized temporal patterns of cortical development, with the greatest increases in unimodal sensorimotor networks and the most prolonged increases in superior and anterior transmodal networks. Notably, we found that executive function was associated with structural features of limbic and association networks. Taken together, this study delineates data-driven patterns of white matter network development that support cognition and align with major axes of brain maturation. Cold Spring Harbor Laboratory 2023-02-10 /pmc/articles/PMC9934602/ /pubmed/36798354 http://dx.doi.org/10.1101/2023.02.09.527696 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Bagautdinova, Joëlle
Bourque, Josiane
Sydnor, Valerie J
Cieslak, Matt
Alexander-Bloch, Aaron F
Bertolero, Max A
Cook, Phil A
Gur, Raquel C
Gur, Ruben E
Larsen, Bart
Moore, Tyler M
Radhakrishnan, Hamsi
Roalf, David R
Shinohara, Russel T
Tapera, Tinashe M
Zhao, Chenying
Sotiras, Aristeidis
Davatzikos, Christos
Satterthwaite, Theodore D
Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth
title Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth
title_full Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth
title_fullStr Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth
title_full_unstemmed Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth
title_short Development of White Matter Fiber Covariance Networks Supports Executive Function in Youth
title_sort development of white matter fiber covariance networks supports executive function in youth
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9934602/
https://www.ncbi.nlm.nih.gov/pubmed/36798354
http://dx.doi.org/10.1101/2023.02.09.527696
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