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Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium

Small average differences in the left-right asymmetry of cerebral cortical thickness have been reported in individuals with autism spectrum disorder (ASD) compared to typically developing controls, affecting widespread cortical regions. The possible impacts of these regional alterations in terms of...

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Autores principales: Sha, Zhiqiang, van Rooij, Daan, Anagnostou, Evdokia, Arango, Celso, Auzias, Guillaume, Behrmann, Marlene, Bernhardt, Boris, Bolte, Sven, Busatto, Geraldo F., Calderoni, Sara, Calvo, Rosa, Daly, Eileen, Deruelle, Christine, Duan, Meiyu, Duran, Fabio Luis Souza, Durston, Sarah, Ecker, Christine, Ehrlich, Stefan, Fair, Damien, Fedor, Jennifer, Fitzgerald, Jacqueline, Floris, Dorothea L., Franke, Barbara, Freitag, Christine M., Gallagher, Louise, Glahn, David C., Haar, Shlomi, Hoekstra, Liesbeth, Jahanshad, Neda, Jalbrzikowski, Maria, Janssen, Joost, King, Joseph A., Lazaro, Luisa, Luna, Beatriz, McGrath, Jane, Medland, Sarah E., Muratori, Filippo, Murphy, Declan G. M., Neufeld, Janina, O’Hearn, Kirsten, Oranje, Bob, Parellada, Mara, Pariente, Jose C., Postema, Merel C., Remnelius, Karl Lundin, Retico, Alessandra, Rosa, Pedro Gomes Penteado, Rubia, Katya, Shook, Devon, Tammimies, Kristiina, Taylor, Margot J., Tosetti, Michela, Wallace, Gregory L., Zhou, Fengfeng, Thompson, Paul M., Fisher, Simon E., Buitelaar, Jan K., Francks, Clyde
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9126820/
https://www.ncbi.nlm.nih.gov/pubmed/35136228
http://dx.doi.org/10.1038/s41380-022-01452-7
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author Sha, Zhiqiang
van Rooij, Daan
Anagnostou, Evdokia
Arango, Celso
Auzias, Guillaume
Behrmann, Marlene
Bernhardt, Boris
Bolte, Sven
Busatto, Geraldo F.
Calderoni, Sara
Calvo, Rosa
Daly, Eileen
Deruelle, Christine
Duan, Meiyu
Duran, Fabio Luis Souza
Durston, Sarah
Ecker, Christine
Ehrlich, Stefan
Fair, Damien
Fedor, Jennifer
Fitzgerald, Jacqueline
Floris, Dorothea L.
Franke, Barbara
Freitag, Christine M.
Gallagher, Louise
Glahn, David C.
Haar, Shlomi
Hoekstra, Liesbeth
Jahanshad, Neda
Jalbrzikowski, Maria
Janssen, Joost
King, Joseph A.
Lazaro, Luisa
Luna, Beatriz
McGrath, Jane
Medland, Sarah E.
Muratori, Filippo
Murphy, Declan G. M.
Neufeld, Janina
O’Hearn, Kirsten
Oranje, Bob
Parellada, Mara
Pariente, Jose C.
Postema, Merel C.
Remnelius, Karl Lundin
Retico, Alessandra
Rosa, Pedro Gomes Penteado
Rubia, Katya
Shook, Devon
Tammimies, Kristiina
Taylor, Margot J.
Tosetti, Michela
Wallace, Gregory L.
Zhou, Fengfeng
Thompson, Paul M.
Fisher, Simon E.
Buitelaar, Jan K.
Francks, Clyde
author_facet Sha, Zhiqiang
van Rooij, Daan
Anagnostou, Evdokia
Arango, Celso
Auzias, Guillaume
Behrmann, Marlene
Bernhardt, Boris
Bolte, Sven
Busatto, Geraldo F.
Calderoni, Sara
Calvo, Rosa
Daly, Eileen
Deruelle, Christine
Duan, Meiyu
Duran, Fabio Luis Souza
Durston, Sarah
Ecker, Christine
Ehrlich, Stefan
Fair, Damien
Fedor, Jennifer
Fitzgerald, Jacqueline
Floris, Dorothea L.
Franke, Barbara
Freitag, Christine M.
Gallagher, Louise
Glahn, David C.
Haar, Shlomi
Hoekstra, Liesbeth
Jahanshad, Neda
Jalbrzikowski, Maria
Janssen, Joost
King, Joseph A.
Lazaro, Luisa
Luna, Beatriz
McGrath, Jane
Medland, Sarah E.
Muratori, Filippo
Murphy, Declan G. M.
Neufeld, Janina
O’Hearn, Kirsten
Oranje, Bob
Parellada, Mara
Pariente, Jose C.
Postema, Merel C.
Remnelius, Karl Lundin
Retico, Alessandra
Rosa, Pedro Gomes Penteado
Rubia, Katya
Shook, Devon
Tammimies, Kristiina
Taylor, Margot J.
Tosetti, Michela
Wallace, Gregory L.
Zhou, Fengfeng
Thompson, Paul M.
Fisher, Simon E.
Buitelaar, Jan K.
Francks, Clyde
author_sort Sha, Zhiqiang
collection PubMed
description Small average differences in the left-right asymmetry of cerebral cortical thickness have been reported in individuals with autism spectrum disorder (ASD) compared to typically developing controls, affecting widespread cortical regions. The possible impacts of these regional alterations in terms of structural network effects have not previously been characterized. Inter-regional morphological covariance analysis can capture network connectivity between different cortical areas at the macroscale level. Here, we used cortical thickness data from 1455 individuals with ASD and 1560 controls, across 43 independent datasets of the ENIGMA consortium’s ASD Working Group, to assess hemispheric asymmetries of intra-individual structural covariance networks, using graph theory-based topological metrics. Compared with typical features of small-world architecture in controls, the ASD sample showed significantly altered average asymmetry of networks involving the fusiform, rostral middle frontal, and medial orbitofrontal cortex, involving higher randomization of the corresponding right-hemispheric networks in ASD. A network involving the superior frontal cortex showed decreased right-hemisphere randomization. Based on comparisons with meta-analyzed functional neuroimaging data, the altered connectivity asymmetry particularly affected networks that subserve executive functions, language-related and sensorimotor processes. These findings provide a network-level characterization of altered left-right brain asymmetry in ASD, based on a large combined sample. Altered asymmetrical brain development in ASD may be partly propagated among spatially distant regions through structural connectivity.
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spelling pubmed-91268202022-05-25 Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium Sha, Zhiqiang van Rooij, Daan Anagnostou, Evdokia Arango, Celso Auzias, Guillaume Behrmann, Marlene Bernhardt, Boris Bolte, Sven Busatto, Geraldo F. Calderoni, Sara Calvo, Rosa Daly, Eileen Deruelle, Christine Duan, Meiyu Duran, Fabio Luis Souza Durston, Sarah Ecker, Christine Ehrlich, Stefan Fair, Damien Fedor, Jennifer Fitzgerald, Jacqueline Floris, Dorothea L. Franke, Barbara Freitag, Christine M. Gallagher, Louise Glahn, David C. Haar, Shlomi Hoekstra, Liesbeth Jahanshad, Neda Jalbrzikowski, Maria Janssen, Joost King, Joseph A. Lazaro, Luisa Luna, Beatriz McGrath, Jane Medland, Sarah E. Muratori, Filippo Murphy, Declan G. M. Neufeld, Janina O’Hearn, Kirsten Oranje, Bob Parellada, Mara Pariente, Jose C. Postema, Merel C. Remnelius, Karl Lundin Retico, Alessandra Rosa, Pedro Gomes Penteado Rubia, Katya Shook, Devon Tammimies, Kristiina Taylor, Margot J. Tosetti, Michela Wallace, Gregory L. Zhou, Fengfeng Thompson, Paul M. Fisher, Simon E. Buitelaar, Jan K. Francks, Clyde Mol Psychiatry Article Small average differences in the left-right asymmetry of cerebral cortical thickness have been reported in individuals with autism spectrum disorder (ASD) compared to typically developing controls, affecting widespread cortical regions. The possible impacts of these regional alterations in terms of structural network effects have not previously been characterized. Inter-regional morphological covariance analysis can capture network connectivity between different cortical areas at the macroscale level. Here, we used cortical thickness data from 1455 individuals with ASD and 1560 controls, across 43 independent datasets of the ENIGMA consortium’s ASD Working Group, to assess hemispheric asymmetries of intra-individual structural covariance networks, using graph theory-based topological metrics. Compared with typical features of small-world architecture in controls, the ASD sample showed significantly altered average asymmetry of networks involving the fusiform, rostral middle frontal, and medial orbitofrontal cortex, involving higher randomization of the corresponding right-hemispheric networks in ASD. A network involving the superior frontal cortex showed decreased right-hemisphere randomization. Based on comparisons with meta-analyzed functional neuroimaging data, the altered connectivity asymmetry particularly affected networks that subserve executive functions, language-related and sensorimotor processes. These findings provide a network-level characterization of altered left-right brain asymmetry in ASD, based on a large combined sample. Altered asymmetrical brain development in ASD may be partly propagated among spatially distant regions through structural connectivity. Nature Publishing Group UK 2022-02-08 2022 /pmc/articles/PMC9126820/ /pubmed/35136228 http://dx.doi.org/10.1038/s41380-022-01452-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sha, Zhiqiang
van Rooij, Daan
Anagnostou, Evdokia
Arango, Celso
Auzias, Guillaume
Behrmann, Marlene
Bernhardt, Boris
Bolte, Sven
Busatto, Geraldo F.
Calderoni, Sara
Calvo, Rosa
Daly, Eileen
Deruelle, Christine
Duan, Meiyu
Duran, Fabio Luis Souza
Durston, Sarah
Ecker, Christine
Ehrlich, Stefan
Fair, Damien
Fedor, Jennifer
Fitzgerald, Jacqueline
Floris, Dorothea L.
Franke, Barbara
Freitag, Christine M.
Gallagher, Louise
Glahn, David C.
Haar, Shlomi
Hoekstra, Liesbeth
Jahanshad, Neda
Jalbrzikowski, Maria
Janssen, Joost
King, Joseph A.
Lazaro, Luisa
Luna, Beatriz
McGrath, Jane
Medland, Sarah E.
Muratori, Filippo
Murphy, Declan G. M.
Neufeld, Janina
O’Hearn, Kirsten
Oranje, Bob
Parellada, Mara
Pariente, Jose C.
Postema, Merel C.
Remnelius, Karl Lundin
Retico, Alessandra
Rosa, Pedro Gomes Penteado
Rubia, Katya
Shook, Devon
Tammimies, Kristiina
Taylor, Margot J.
Tosetti, Michela
Wallace, Gregory L.
Zhou, Fengfeng
Thompson, Paul M.
Fisher, Simon E.
Buitelaar, Jan K.
Francks, Clyde
Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium
title Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium
title_full Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium
title_fullStr Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium
title_full_unstemmed Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium
title_short Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium
title_sort subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the enigma consortium
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9126820/
https://www.ncbi.nlm.nih.gov/pubmed/35136228
http://dx.doi.org/10.1038/s41380-022-01452-7
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