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Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking

In athletes, long‐term intensive training has been shown to increase unparalleled athletic ability and might induce brain plasticity. We evaluated the structural connectome of world‐class gymnasts (WCGs), as mapped by diffusion‐weighted magnetic resonance imaging probabilistic tractography and a mul...

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Autores principales: Tomita, Hiroyuki, Kamagata, Koji, Andica, Christina, Uchida, Wataru, Fukuo, Makoto, Waki, Hidefumi, Sugano, Hidenori, Tange, Yuichi, Mitsuhashi, Takumi, Lukies, Matthew, Hagiwara, Akifumi, Fujita, Shohei, Wada, Akihiko, Akashi, Toshiaki, Murata, Syo, Harada, Mutsumi, Aoki, Shigeki, Naito, Hisashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541483/
https://www.ncbi.nlm.nih.gov/pubmed/34245603
http://dx.doi.org/10.1002/jnr.24912
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author Tomita, Hiroyuki
Kamagata, Koji
Andica, Christina
Uchida, Wataru
Fukuo, Makoto
Waki, Hidefumi
Sugano, Hidenori
Tange, Yuichi
Mitsuhashi, Takumi
Lukies, Matthew
Hagiwara, Akifumi
Fujita, Shohei
Wada, Akihiko
Akashi, Toshiaki
Murata, Syo
Harada, Mutsumi
Aoki, Shigeki
Naito, Hisashi
author_facet Tomita, Hiroyuki
Kamagata, Koji
Andica, Christina
Uchida, Wataru
Fukuo, Makoto
Waki, Hidefumi
Sugano, Hidenori
Tange, Yuichi
Mitsuhashi, Takumi
Lukies, Matthew
Hagiwara, Akifumi
Fujita, Shohei
Wada, Akihiko
Akashi, Toshiaki
Murata, Syo
Harada, Mutsumi
Aoki, Shigeki
Naito, Hisashi
author_sort Tomita, Hiroyuki
collection PubMed
description In athletes, long‐term intensive training has been shown to increase unparalleled athletic ability and might induce brain plasticity. We evaluated the structural connectome of world‐class gymnasts (WCGs), as mapped by diffusion‐weighted magnetic resonance imaging probabilistic tractography and a multishell, multitissue constrained spherical deconvolution method to increase the precision of tractography at the tissue interfaces. The connectome was mapped in 10 Japanese male WCGs and in 10 age‐matched male controls. Network‐based statistic identified subnetworks with increased connectivity density in WCGs, involving the sensorimotor, default mode, attentional, visual, and limbic areas. It also revealed a significant association between the structural connectivity of some brain structures with functions closely related to the gymnastic skills and the D‐score, which is used as an index of the gymnasts' specific physical abilities for each apparatus. Furthermore, graph theory analysis demonstrated the characteristics of brain anatomical topology in the WCGs. They displayed significantly increased global connectivity strength with decreased characteristic path length at the global level and higher nodal strength and degree in the sensorimotor, default mode, attention, and limbic/subcortical areas at the local level as compared with controls. Together, these findings extend the current understanding of neural mechanisms that distinguish WCGs from controls and suggest brain anatomical network plasticity in WCGs resulting from long‐term intensive training. Future studies should assess the contribution of genetic or early‐life environmental factors in the brain network organization of WCGs. Furthermore, the indices of brain topology (i.e., connection density and graph theory indices) could become markers for the objective evaluation of gymnastic performance.
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spelling pubmed-95414832022-10-14 Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking Tomita, Hiroyuki Kamagata, Koji Andica, Christina Uchida, Wataru Fukuo, Makoto Waki, Hidefumi Sugano, Hidenori Tange, Yuichi Mitsuhashi, Takumi Lukies, Matthew Hagiwara, Akifumi Fujita, Shohei Wada, Akihiko Akashi, Toshiaki Murata, Syo Harada, Mutsumi Aoki, Shigeki Naito, Hisashi J Neurosci Res Research Articles In athletes, long‐term intensive training has been shown to increase unparalleled athletic ability and might induce brain plasticity. We evaluated the structural connectome of world‐class gymnasts (WCGs), as mapped by diffusion‐weighted magnetic resonance imaging probabilistic tractography and a multishell, multitissue constrained spherical deconvolution method to increase the precision of tractography at the tissue interfaces. The connectome was mapped in 10 Japanese male WCGs and in 10 age‐matched male controls. Network‐based statistic identified subnetworks with increased connectivity density in WCGs, involving the sensorimotor, default mode, attentional, visual, and limbic areas. It also revealed a significant association between the structural connectivity of some brain structures with functions closely related to the gymnastic skills and the D‐score, which is used as an index of the gymnasts' specific physical abilities for each apparatus. Furthermore, graph theory analysis demonstrated the characteristics of brain anatomical topology in the WCGs. They displayed significantly increased global connectivity strength with decreased characteristic path length at the global level and higher nodal strength and degree in the sensorimotor, default mode, attention, and limbic/subcortical areas at the local level as compared with controls. Together, these findings extend the current understanding of neural mechanisms that distinguish WCGs from controls and suggest brain anatomical network plasticity in WCGs resulting from long‐term intensive training. Future studies should assess the contribution of genetic or early‐life environmental factors in the brain network organization of WCGs. Furthermore, the indices of brain topology (i.e., connection density and graph theory indices) could become markers for the objective evaluation of gymnastic performance. John Wiley and Sons Inc. 2021-07-10 2021-10 /pmc/articles/PMC9541483/ /pubmed/34245603 http://dx.doi.org/10.1002/jnr.24912 Text en © 2021 The Authors. Journal of Neuroscience Research published by Wiley Periodicals LLC https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Tomita, Hiroyuki
Kamagata, Koji
Andica, Christina
Uchida, Wataru
Fukuo, Makoto
Waki, Hidefumi
Sugano, Hidenori
Tange, Yuichi
Mitsuhashi, Takumi
Lukies, Matthew
Hagiwara, Akifumi
Fujita, Shohei
Wada, Akihiko
Akashi, Toshiaki
Murata, Syo
Harada, Mutsumi
Aoki, Shigeki
Naito, Hisashi
Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
title Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
title_full Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
title_fullStr Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
title_full_unstemmed Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
title_short Connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
title_sort connectome analysis of male world‐class gymnasts using probabilistic multishell, multitissue constrained spherical deconvolution tracking
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541483/
https://www.ncbi.nlm.nih.gov/pubmed/34245603
http://dx.doi.org/10.1002/jnr.24912
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