Brain-computer-interface-based intervention re-normalizes brain functional network topology in children with attention deficit/hyperactivity disorder
A brain-computer-interface (BCI)-based attention training game system has shown promise for treating attention deficit/hyperactivity disorder (ADHD) children with inattentive symptoms. However, little is known about brain network organizational changes underlying behavior improvement following BCI-b...
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creator | Qian, Xing Loo, Beatrice Rui Yi Castellanos, Francisco Xavier Liu, Siwei Koh, Hui Li Poh, Xue Wei Wendy Krishnan, Ranga Fung, Daniel Chee, Michael WL Guan, Cuntai Lee, Tih-Shih Lim, Choon Guan Zhou, Juan |
description | A brain-computer-interface (BCI)-based attention training game system has shown promise for treating attention deficit/hyperactivity disorder (ADHD) children with inattentive symptoms. However, little is known about brain network organizational changes underlying behavior improvement following BCI-based training. To cover this gap, we aimed to examine the topological alterations of large-scale brain functional networks induced by the 8-week BCI-based attention intervention in ADHD boys using resting-state functional magnetic resonance imaging method. Compared to the non-intervention (ADHD-NI) group, the intervention group (ADHD-I) showed greater reduction of inattention symptoms accompanied with differential brain network reorganizations after training. Specifically, the ADHD-NI group had increased functional connectivity (FC) within the salience/ventral attention network (SVN) and increased FC between task-positive networks (including the SVN, dorsal attention (DAN), somatomotor, and executive control network) and subcortical regions; in contrast ADHD-I group did not have this pattern. In parallel, ADHD-I group had reduced degree centrality and clustering coefficient as well as increased closeness in task-positive and the default mode networks (prefrontal regions) after the training. More importantly, these reduced local functional processing mainly in the SVN were associated with less inattentive/internalizing problems after 8-week BCI-based intervention across ADHD patients. Our findings suggest that the BCI-based attention training facilitates behavioral improvement in ADHD children by reorganizing brain functional network from more regular to more random configurations, particularly renormalizing salience network processing. Future long-term longitudinal neuroimaging studies are needed to develop the BCI-based intervention approach to promote brain maturation in ADHD. |
doi_str_mv | 10.1038/s41398-018-0213-8 |
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However, little is known about brain network organizational changes underlying behavior improvement following BCI-based training. To cover this gap, we aimed to examine the topological alterations of large-scale brain functional networks induced by the 8-week BCI-based attention intervention in ADHD boys using resting-state functional magnetic resonance imaging method. Compared to the non-intervention (ADHD-NI) group, the intervention group (ADHD-I) showed greater reduction of inattention symptoms accompanied with differential brain network reorganizations after training. Specifically, the ADHD-NI group had increased functional connectivity (FC) within the salience/ventral attention network (SVN) and increased FC between task-positive networks (including the SVN, dorsal attention (DAN), somatomotor, and executive control network) and subcortical regions; in contrast ADHD-I group did not have this pattern. In parallel, ADHD-I group had reduced degree centrality and clustering coefficient as well as increased closeness in task-positive and the default mode networks (prefrontal regions) after the training. More importantly, these reduced local functional processing mainly in the SVN were associated with less inattentive/internalizing problems after 8-week BCI-based intervention across ADHD patients. Our findings suggest that the BCI-based attention training facilitates behavioral improvement in ADHD children by reorganizing brain functional network from more regular to more random configurations, particularly renormalizing salience network processing. Future long-term longitudinal neuroimaging studies are needed to develop the BCI-based intervention approach to promote brain maturation in ADHD.</description><identifier>ISSN: 2158-3188</identifier><identifier>EISSN: 2158-3188</identifier><identifier>DOI: 10.1038/s41398-018-0213-8</identifier><identifier>PMID: 30097579</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>59/36 ; 59/57 ; 631/477/2811 ; 692/699/476/1311 ; Attention Deficit Disorder with Hyperactivity - psychology ; Attention Deficit Disorder with Hyperactivity - rehabilitation ; Attention Deficit Hyperactivity Disorder ; Behavioral Sciences ; Biological Psychology ; Brain - diagnostic imaging ; Brain - physiopathology ; Brain Mapping ; Brain-Computer Interfaces ; Child ; Cluster Analysis ; Defense Mechanisms ; Executive Function ; Humans ; Magnetic Resonance Imaging ; Male ; Medicine ; Medicine & Public Health ; Neural Pathways ; Neurosciences ; Pharmacotherapy ; Psychiatry ; Psychomotor Agitation ; Singapore</subject><ispartof>Translational psychiatry, 2018-08, Vol.8 (1), p.149-11, Article 149</ispartof><rights>The Author(s) 2018</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-261642bad7dc3ce71beed50c49fe822d75311639aef795764875a799b17931b93</citedby><cites>FETCH-LOGICAL-c470t-261642bad7dc3ce71beed50c49fe822d75311639aef795764875a799b17931b93</cites><orcidid>0000-0002-0180-8648 ; 0000-0002-6087-0548</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6086861/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6086861/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,27929,27930,41125,42194,51581,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30097579$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Qian, Xing</creatorcontrib><creatorcontrib>Loo, Beatrice Rui Yi</creatorcontrib><creatorcontrib>Castellanos, Francisco Xavier</creatorcontrib><creatorcontrib>Liu, Siwei</creatorcontrib><creatorcontrib>Koh, Hui Li</creatorcontrib><creatorcontrib>Poh, Xue Wei Wendy</creatorcontrib><creatorcontrib>Krishnan, Ranga</creatorcontrib><creatorcontrib>Fung, Daniel</creatorcontrib><creatorcontrib>Chee, Michael WL</creatorcontrib><creatorcontrib>Guan, Cuntai</creatorcontrib><creatorcontrib>Lee, Tih-Shih</creatorcontrib><creatorcontrib>Lim, Choon Guan</creatorcontrib><creatorcontrib>Zhou, Juan</creatorcontrib><title>Brain-computer-interface-based intervention re-normalizes brain functional network topology in children with attention deficit/hyperactivity disorder</title><title>Translational psychiatry</title><addtitle>Transl Psychiatry</addtitle><addtitle>Transl Psychiatry</addtitle><description>A brain-computer-interface (BCI)-based attention training game system has shown promise for treating attention deficit/hyperactivity disorder (ADHD) children with inattentive symptoms. However, little is known about brain network organizational changes underlying behavior improvement following BCI-based training. To cover this gap, we aimed to examine the topological alterations of large-scale brain functional networks induced by the 8-week BCI-based attention intervention in ADHD boys using resting-state functional magnetic resonance imaging method. Compared to the non-intervention (ADHD-NI) group, the intervention group (ADHD-I) showed greater reduction of inattention symptoms accompanied with differential brain network reorganizations after training. Specifically, the ADHD-NI group had increased functional connectivity (FC) within the salience/ventral attention network (SVN) and increased FC between task-positive networks (including the SVN, dorsal attention (DAN), somatomotor, and executive control network) and subcortical regions; in contrast ADHD-I group did not have this pattern. In parallel, ADHD-I group had reduced degree centrality and clustering coefficient as well as increased closeness in task-positive and the default mode networks (prefrontal regions) after the training. More importantly, these reduced local functional processing mainly in the SVN were associated with less inattentive/internalizing problems after 8-week BCI-based intervention across ADHD patients. Our findings suggest that the BCI-based attention training facilitates behavioral improvement in ADHD children by reorganizing brain functional network from more regular to more random configurations, particularly renormalizing salience network processing. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Translational psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Qian, Xing</au><au>Loo, Beatrice Rui Yi</au><au>Castellanos, Francisco Xavier</au><au>Liu, Siwei</au><au>Koh, Hui Li</au><au>Poh, Xue Wei Wendy</au><au>Krishnan, Ranga</au><au>Fung, Daniel</au><au>Chee, Michael WL</au><au>Guan, Cuntai</au><au>Lee, Tih-Shih</au><au>Lim, Choon Guan</au><au>Zhou, Juan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brain-computer-interface-based intervention re-normalizes brain functional network topology in children with attention deficit/hyperactivity disorder</atitle><jtitle>Translational psychiatry</jtitle><stitle>Transl Psychiatry</stitle><addtitle>Transl Psychiatry</addtitle><date>2018-08-10</date><risdate>2018</risdate><volume>8</volume><issue>1</issue><spage>149</spage><epage>11</epage><pages>149-11</pages><artnum>149</artnum><issn>2158-3188</issn><eissn>2158-3188</eissn><abstract>A brain-computer-interface (BCI)-based attention training game system has shown promise for treating attention deficit/hyperactivity disorder (ADHD) children with inattentive symptoms. However, little is known about brain network organizational changes underlying behavior improvement following BCI-based training. To cover this gap, we aimed to examine the topological alterations of large-scale brain functional networks induced by the 8-week BCI-based attention intervention in ADHD boys using resting-state functional magnetic resonance imaging method. Compared to the non-intervention (ADHD-NI) group, the intervention group (ADHD-I) showed greater reduction of inattention symptoms accompanied with differential brain network reorganizations after training. Specifically, the ADHD-NI group had increased functional connectivity (FC) within the salience/ventral attention network (SVN) and increased FC between task-positive networks (including the SVN, dorsal attention (DAN), somatomotor, and executive control network) and subcortical regions; in contrast ADHD-I group did not have this pattern. In parallel, ADHD-I group had reduced degree centrality and clustering coefficient as well as increased closeness in task-positive and the default mode networks (prefrontal regions) after the training. More importantly, these reduced local functional processing mainly in the SVN were associated with less inattentive/internalizing problems after 8-week BCI-based intervention across ADHD patients. Our findings suggest that the BCI-based attention training facilitates behavioral improvement in ADHD children by reorganizing brain functional network from more regular to more random configurations, particularly renormalizing salience network processing. Future long-term longitudinal neuroimaging studies are needed to develop the BCI-based intervention approach to promote brain maturation in ADHD.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30097579</pmid><doi>10.1038/s41398-018-0213-8</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-0180-8648</orcidid><orcidid>https://orcid.org/0000-0002-6087-0548</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 59/36 59/57 631/477/2811 692/699/476/1311 Attention Deficit Disorder with Hyperactivity - psychology Attention Deficit Disorder with Hyperactivity - rehabilitation Attention Deficit Hyperactivity Disorder Behavioral Sciences Biological Psychology Brain - diagnostic imaging Brain - physiopathology Brain Mapping Brain-Computer Interfaces Child Cluster Analysis Defense Mechanisms Executive Function Humans Magnetic Resonance Imaging Male Medicine Medicine & Public Health Neural Pathways Neurosciences Pharmacotherapy Psychiatry Psychomotor Agitation Singapore |
title | Brain-computer-interface-based intervention re-normalizes brain functional network topology in children with attention deficit/hyperactivity disorder |
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