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Optimization of energy state transition trajectory supports the development of executive function during youth

Executive function develops during adolescence, yet it remains unknown how structural brain networks mature to facilitate activation of the fronto-parietal system, which is critical for executive function. In a sample of 946 human youths (ages 8-23y) who completed diffusion imaging, we capitalized u...

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Autores principales: Cui, Zaixu, Stiso, Jennifer, Baum, Graham L, Kim, Jason Z, Roalf, David R, Betzel, Richard F, Gu, Shi, Lu, Zhixin, Xia, Cedric H, He, Xiaosong, Ciric, Rastko, Oathes, Desmond J, Moore, Tyler M, Shinohara, Russell T, Ruparel, Kosha, Davatzikos, Christos, Pasqualetti, Fabio, Gur, Raquel E, Gur, Ruben C, Bassett, Danielle S, Satterthwaite, Theodore D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162657/
https://www.ncbi.nlm.nih.gov/pubmed/32216874
http://dx.doi.org/10.7554/eLife.53060
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author Cui, Zaixu
Stiso, Jennifer
Baum, Graham L
Kim, Jason Z
Roalf, David R
Betzel, Richard F
Gu, Shi
Lu, Zhixin
Xia, Cedric H
He, Xiaosong
Ciric, Rastko
Oathes, Desmond J
Moore, Tyler M
Shinohara, Russell T
Ruparel, Kosha
Davatzikos, Christos
Pasqualetti, Fabio
Gur, Raquel E
Gur, Ruben C
Bassett, Danielle S
Satterthwaite, Theodore D
author_facet Cui, Zaixu
Stiso, Jennifer
Baum, Graham L
Kim, Jason Z
Roalf, David R
Betzel, Richard F
Gu, Shi
Lu, Zhixin
Xia, Cedric H
He, Xiaosong
Ciric, Rastko
Oathes, Desmond J
Moore, Tyler M
Shinohara, Russell T
Ruparel, Kosha
Davatzikos, Christos
Pasqualetti, Fabio
Gur, Raquel E
Gur, Ruben C
Bassett, Danielle S
Satterthwaite, Theodore D
author_sort Cui, Zaixu
collection PubMed
description Executive function develops during adolescence, yet it remains unknown how structural brain networks mature to facilitate activation of the fronto-parietal system, which is critical for executive function. In a sample of 946 human youths (ages 8-23y) who completed diffusion imaging, we capitalized upon recent advances in linear dynamical network control theory to calculate the energetic cost necessary to activate the fronto-parietal system through the control of multiple brain regions given existing structural network topology. We found that the energy required to activate the fronto-parietal system declined with development, and the pattern of regional energetic cost predicts unseen individuals’ brain maturity. Finally, energetic requirements of the cingulate cortex were negatively correlated with executive performance, and partially mediated the development of executive performance with age. Our results reveal a mechanism by which structural networks develop during adolescence to reduce the theoretical energetic costs of transitions to activation states necessary for executive function.
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spelling pubmed-71626572020-04-20 Optimization of energy state transition trajectory supports the development of executive function during youth Cui, Zaixu Stiso, Jennifer Baum, Graham L Kim, Jason Z Roalf, David R Betzel, Richard F Gu, Shi Lu, Zhixin Xia, Cedric H He, Xiaosong Ciric, Rastko Oathes, Desmond J Moore, Tyler M Shinohara, Russell T Ruparel, Kosha Davatzikos, Christos Pasqualetti, Fabio Gur, Raquel E Gur, Ruben C Bassett, Danielle S Satterthwaite, Theodore D eLife Neuroscience Executive function develops during adolescence, yet it remains unknown how structural brain networks mature to facilitate activation of the fronto-parietal system, which is critical for executive function. In a sample of 946 human youths (ages 8-23y) who completed diffusion imaging, we capitalized upon recent advances in linear dynamical network control theory to calculate the energetic cost necessary to activate the fronto-parietal system through the control of multiple brain regions given existing structural network topology. We found that the energy required to activate the fronto-parietal system declined with development, and the pattern of regional energetic cost predicts unseen individuals’ brain maturity. Finally, energetic requirements of the cingulate cortex were negatively correlated with executive performance, and partially mediated the development of executive performance with age. Our results reveal a mechanism by which structural networks develop during adolescence to reduce the theoretical energetic costs of transitions to activation states necessary for executive function. eLife Sciences Publications, Ltd 2020-03-27 /pmc/articles/PMC7162657/ /pubmed/32216874 http://dx.doi.org/10.7554/eLife.53060 Text en © 2020, Cui et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Cui, Zaixu
Stiso, Jennifer
Baum, Graham L
Kim, Jason Z
Roalf, David R
Betzel, Richard F
Gu, Shi
Lu, Zhixin
Xia, Cedric H
He, Xiaosong
Ciric, Rastko
Oathes, Desmond J
Moore, Tyler M
Shinohara, Russell T
Ruparel, Kosha
Davatzikos, Christos
Pasqualetti, Fabio
Gur, Raquel E
Gur, Ruben C
Bassett, Danielle S
Satterthwaite, Theodore D
Optimization of energy state transition trajectory supports the development of executive function during youth
title Optimization of energy state transition trajectory supports the development of executive function during youth
title_full Optimization of energy state transition trajectory supports the development of executive function during youth
title_fullStr Optimization of energy state transition trajectory supports the development of executive function during youth
title_full_unstemmed Optimization of energy state transition trajectory supports the development of executive function during youth
title_short Optimization of energy state transition trajectory supports the development of executive function during youth
title_sort optimization of energy state transition trajectory supports the development of executive function during youth
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162657/
https://www.ncbi.nlm.nih.gov/pubmed/32216874
http://dx.doi.org/10.7554/eLife.53060
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