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Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder

BACKGROUND: Previous neuroimaging studies have described shared and distinct neurobiological mechanisms between autism spectrum disorders (ASDs) and attention-deficit/hyperactivity disorder (ADHD). However, little is known about the similarities and differences in topologically structural connectivi...

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Autores principales: Qian, Lu, Li, Yun, Wang, Yao, Wang, Yue, Cheng, Xin, Li, Chunyan, Cui, Xiwen, Jiao, Gongkai, Ke, Xiaoyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8226092/
https://www.ncbi.nlm.nih.gov/pubmed/34177449
http://dx.doi.org/10.3389/fnins.2021.664363
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author Qian, Lu
Li, Yun
Wang, Yao
Wang, Yue
Cheng, Xin
Li, Chunyan
Cui, Xiwen
Jiao, Gongkai
Ke, Xiaoyan
author_facet Qian, Lu
Li, Yun
Wang, Yao
Wang, Yue
Cheng, Xin
Li, Chunyan
Cui, Xiwen
Jiao, Gongkai
Ke, Xiaoyan
author_sort Qian, Lu
collection PubMed
description BACKGROUND: Previous neuroimaging studies have described shared and distinct neurobiological mechanisms between autism spectrum disorders (ASDs) and attention-deficit/hyperactivity disorder (ADHD). However, little is known about the similarities and differences in topologically structural connectivity patterns between the two disorders. METHODS: Diffusion tensor imaging (DTI) and deterministic tractography were used to construct the brain white matter (WM) structural networks of children and adolescents (age range, 6–16 years); 31 had ASD, 34 had ADHD, and 30 were age- and sex-matched typically developing (TD) individuals. Then, graph theoretical analysis was performed to investigate the alterations in the global and node-based properties of the WM structural networks in these groups. Next, measures of ASD traits [Social Responsiveness Scale (SRS)] and ADHD traits (Swanson, Nolan, and Pelham, version IV scale, SNAP-IV) were correlated with the alterations to determine the functional significance of such changes. RESULTS: First, there were no significant differences in the global network properties among the three groups; moreover, compared with that of the TD group, nodal degree (Ki) of the right amygdala (AMYG.R) and right parahippocampal gyrus (PHG.R) were found in both the ASD and ADHD groups. Also, the ASD and ADHD groups shared four additional hubs, including the left middle temporal gyrus (MTG.L), left superior temporal gyrus (STG.L), left postcentral gyrus (PoCG.L), and right middle frontal gyrus (MFG.R) compared with the TD group. Moreover, the ASD and ADHD groups exhibited no significant differences regarding regional connectivity characteristics. Second, the ADHD group showed significantly increased nodal betweenness centrality (Bi) of the left hippocampus (HIP.L) compared with the ASD group; also, compared with the ADHD group, the ASD group lacked the left anterior cingulate gyrus (ACG.L) as a hub. Last, decreased nodal efficiency (Enodal) of the AMYG.R, Ki of the AMYG.R, and Ki of the PHG.R were associated with higher SRS scores in the ASD group. Decreased Ki of the PHG.R was associated with higher SRS scores in the full sample, whereas decreased Bi of the PHG.R was associated with lower oppositional defiance subscale scores of the SNAP-IV in the ADHD group, and decreased Bi of the HIP.L was associated with lower inattention subscale scores of the SNAP-IV in the full sample. CONCLUSION: From the perspective of the topological properties of brain WM structural networks, ADHD and ASD have both shared and distinct features. More interestingly, some shared and distinct topological properties of WM structures are related to the core symptoms of these disorders.
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spelling pubmed-82260922021-06-26 Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Qian, Lu Li, Yun Wang, Yao Wang, Yue Cheng, Xin Li, Chunyan Cui, Xiwen Jiao, Gongkai Ke, Xiaoyan Front Neurosci Neuroscience BACKGROUND: Previous neuroimaging studies have described shared and distinct neurobiological mechanisms between autism spectrum disorders (ASDs) and attention-deficit/hyperactivity disorder (ADHD). However, little is known about the similarities and differences in topologically structural connectivity patterns between the two disorders. METHODS: Diffusion tensor imaging (DTI) and deterministic tractography were used to construct the brain white matter (WM) structural networks of children and adolescents (age range, 6–16 years); 31 had ASD, 34 had ADHD, and 30 were age- and sex-matched typically developing (TD) individuals. Then, graph theoretical analysis was performed to investigate the alterations in the global and node-based properties of the WM structural networks in these groups. Next, measures of ASD traits [Social Responsiveness Scale (SRS)] and ADHD traits (Swanson, Nolan, and Pelham, version IV scale, SNAP-IV) were correlated with the alterations to determine the functional significance of such changes. RESULTS: First, there were no significant differences in the global network properties among the three groups; moreover, compared with that of the TD group, nodal degree (Ki) of the right amygdala (AMYG.R) and right parahippocampal gyrus (PHG.R) were found in both the ASD and ADHD groups. Also, the ASD and ADHD groups shared four additional hubs, including the left middle temporal gyrus (MTG.L), left superior temporal gyrus (STG.L), left postcentral gyrus (PoCG.L), and right middle frontal gyrus (MFG.R) compared with the TD group. Moreover, the ASD and ADHD groups exhibited no significant differences regarding regional connectivity characteristics. Second, the ADHD group showed significantly increased nodal betweenness centrality (Bi) of the left hippocampus (HIP.L) compared with the ASD group; also, compared with the ADHD group, the ASD group lacked the left anterior cingulate gyrus (ACG.L) as a hub. Last, decreased nodal efficiency (Enodal) of the AMYG.R, Ki of the AMYG.R, and Ki of the PHG.R were associated with higher SRS scores in the ASD group. Decreased Ki of the PHG.R was associated with higher SRS scores in the full sample, whereas decreased Bi of the PHG.R was associated with lower oppositional defiance subscale scores of the SNAP-IV in the ADHD group, and decreased Bi of the HIP.L was associated with lower inattention subscale scores of the SNAP-IV in the full sample. CONCLUSION: From the perspective of the topological properties of brain WM structural networks, ADHD and ASD have both shared and distinct features. More interestingly, some shared and distinct topological properties of WM structures are related to the core symptoms of these disorders. Frontiers Media S.A. 2021-06-11 /pmc/articles/PMC8226092/ /pubmed/34177449 http://dx.doi.org/10.3389/fnins.2021.664363 Text en Copyright © 2021 Qian, Li, Wang, Wang, Cheng, Li, Cui, Jiao and Ke. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Qian, Lu
Li, Yun
Wang, Yao
Wang, Yue
Cheng, Xin
Li, Chunyan
Cui, Xiwen
Jiao, Gongkai
Ke, Xiaoyan
Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder
title Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder
title_full Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder
title_fullStr Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder
title_full_unstemmed Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder
title_short Shared and Distinct Topologically Structural Connectivity Patterns in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder
title_sort shared and distinct topologically structural connectivity patterns in autism spectrum disorder and attention-deficit/hyperactivity disorder
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8226092/
https://www.ncbi.nlm.nih.gov/pubmed/34177449
http://dx.doi.org/10.3389/fnins.2021.664363
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