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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...
Autores principales: | , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2020
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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. |
format | Online Article Text |
id | pubmed-7162657 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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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