Function–structure coupling: White matter functional magnetic resonance imaging hyper‐activation associates with structural integrity reductions in schizophrenia
White matter (WM) microstructure deficit may be an underlying factor in the brain dysconnectivity hypothesis of schizophrenia using diffusion tensor imaging (DTI). However, WM dysfunction is unclear in schizophrenia. This study aimed to investigate the association between structural deficits and fun...
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description | White matter (WM) microstructure deficit may be an underlying factor in the brain dysconnectivity hypothesis of schizophrenia using diffusion tensor imaging (DTI). However, WM dysfunction is unclear in schizophrenia. This study aimed to investigate the association between structural deficits and functional disturbances in major WM tracts in schizophrenia. Using functional magnetic resonance imaging (fMRI) and DTI, we developed the skeleton‐based WM functional analysis, which could achieve voxel‐wise function–structure coupling by projecting the fMRI signals onto a skeleton in WM. We measured the fractional anisotropy (FA) and WM low‐frequency oscillation (LFO) and their couplings in 93 schizophrenia patients and 122 healthy controls (HCs). An independent open database (62 schizophrenia patients and 71 HCs) was used to test the reproducibility. Finally, associations between WM LFO and five behaviour assessment categories (cognition, emotion, motor, personality and sensory) were examined. This study revealed a reversed pattern of structure and function in frontotemporal tracts, as follows. (a) WM hyper‐LFO was associated with reduced FA in schizophrenia. (b) The function–structure association was positive in HCs but negative in schizophrenia patients. Furthermore, function–structure dissociation was exacerbated by long illness duration and severe negative symptoms. (c) WM activations were significantly related to cognition and emotion. This study indicated function–structure dys‐coupling, with higher LFO and reduced structural integration in frontotemporal WM, which may reflect a potential mechanism in WM neuropathologic processing of schizophrenia.
Hyper‐activation of white matter associates with loss of white matter integrity in patients with schizophrenia. The function–structure dys‐coupling exacerbated with long illness duration and severe negative symptoms in schizophrenia, and also associated with cognition and emotion. |
doi_str_mv | 10.1002/hbm.25536 |
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Hyper‐activation of white matter associates with loss of white matter integrity in patients with schizophrenia. The function–structure dys‐coupling exacerbated with long illness duration and severe negative symptoms in schizophrenia, and also associated with cognition and emotion.</description><identifier>ISSN: 1065-9471</identifier><identifier>EISSN: 1097-0193</identifier><identifier>DOI: 10.1002/hbm.25536</identifier><identifier>PMID: 34110075</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>activation ; Adult ; Anisotropy ; Brain ; Brain mapping ; Cognition ; Couplings ; Data processing ; Diffusion Tensor Imaging ; Emotional behavior ; Emotions ; Female ; fMRI ; frontal ; Functional analysis ; Functional magnetic resonance imaging ; Functional Neuroimaging ; Humans ; Magnetic Resonance Imaging ; Male ; Medical imaging ; Mental disorders ; Middle Aged ; Neuroimaging ; Resonance ; Schizophrenia ; Schizophrenia - diagnostic imaging ; Schizophrenia - pathology ; Schizophrenia - physiopathology ; Somatotropin ; Structural integrity ; Structure-function relationships ; Substantia alba ; Tensors ; Time series ; white matter ; White Matter - diagnostic imaging ; White Matter - pathology ; White Matter - physiopathology</subject><ispartof>Human brain mapping, 2021-08, Vol.42 (12), p.4022-4034</ispartof><rights>2021 The Authors. published by Wiley Periodicals LLC.</rights><rights>2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.</rights><rights>COPYRIGHT 2021 John Wiley & Sons, Inc.</rights><rights>2021. This article is published under http://creativecommons.org/licenses/by-nc/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-c5106-fa23b55065b96214910194ff61cb6ba01282a31d86b284a877496c8cd7dc20103</citedby><cites>FETCH-LOGICAL-c5106-fa23b55065b96214910194ff61cb6ba01282a31d86b284a877496c8cd7dc20103</cites><orcidid>0000-0001-7012-0559 ; 0000-0003-0524-5886</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/PMC8288085/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8288085/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,1412,11543,27905,27906,45555,45556,46033,46457,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34110075$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Yuchao</creatorcontrib><creatorcontrib>Duan, Mingjun</creatorcontrib><creatorcontrib>Li, Xiangkui</creatorcontrib><creatorcontrib>Huang, Huan</creatorcontrib><creatorcontrib>Zhao, Guocheng</creatorcontrib><creatorcontrib>Li, Xuan</creatorcontrib><creatorcontrib>Li, Shicai</creatorcontrib><creatorcontrib>Song, Xufeng</creatorcontrib><creatorcontrib>He, Hui</creatorcontrib><creatorcontrib>Yao, Dezhong</creatorcontrib><creatorcontrib>Luo, Cheng</creatorcontrib><title>Function–structure coupling: White matter functional magnetic resonance imaging hyper‐activation associates with structural integrity reductions in schizophrenia</title><title>Human brain mapping</title><addtitle>Hum Brain Mapp</addtitle><description>White matter (WM) microstructure deficit may be an underlying factor in the brain dysconnectivity hypothesis of schizophrenia using diffusion tensor imaging (DTI). However, WM dysfunction is unclear in schizophrenia. This study aimed to investigate the association between structural deficits and functional disturbances in major WM tracts in schizophrenia. Using functional magnetic resonance imaging (fMRI) and DTI, we developed the skeleton‐based WM functional analysis, which could achieve voxel‐wise function–structure coupling by projecting the fMRI signals onto a skeleton in WM. We measured the fractional anisotropy (FA) and WM low‐frequency oscillation (LFO) and their couplings in 93 schizophrenia patients and 122 healthy controls (HCs). An independent open database (62 schizophrenia patients and 71 HCs) was used to test the reproducibility. Finally, associations between WM LFO and five behaviour assessment categories (cognition, emotion, motor, personality and sensory) were examined. This study revealed a reversed pattern of structure and function in frontotemporal tracts, as follows. (a) WM hyper‐LFO was associated with reduced FA in schizophrenia. (b) The function–structure association was positive in HCs but negative in schizophrenia patients. Furthermore, function–structure dissociation was exacerbated by long illness duration and severe negative symptoms. (c) WM activations were significantly related to cognition and emotion. This study indicated function–structure dys‐coupling, with higher LFO and reduced structural integration in frontotemporal WM, which may reflect a potential mechanism in WM neuropathologic processing of schizophrenia.
Hyper‐activation of white matter associates with loss of white matter integrity in patients with schizophrenia. The function–structure dys‐coupling exacerbated with long illness duration and severe negative symptoms in schizophrenia, and also associated with cognition and emotion.</description><subject>activation</subject><subject>Adult</subject><subject>Anisotropy</subject><subject>Brain</subject><subject>Brain mapping</subject><subject>Cognition</subject><subject>Couplings</subject><subject>Data processing</subject><subject>Diffusion Tensor Imaging</subject><subject>Emotional behavior</subject><subject>Emotions</subject><subject>Female</subject><subject>fMRI</subject><subject>frontal</subject><subject>Functional analysis</subject><subject>Functional magnetic resonance imaging</subject><subject>Functional Neuroimaging</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Mental disorders</subject><subject>Middle Aged</subject><subject>Neuroimaging</subject><subject>Resonance</subject><subject>Schizophrenia</subject><subject>Schizophrenia - diagnostic imaging</subject><subject>Schizophrenia - pathology</subject><subject>Schizophrenia - physiopathology</subject><subject>Somatotropin</subject><subject>Structural integrity</subject><subject>Structure-function relationships</subject><subject>Substantia alba</subject><subject>Tensors</subject><subject>Time series</subject><subject>white matter</subject><subject>White Matter - diagnostic imaging</subject><subject>White Matter - pathology</subject><subject>White Matter - physiopathology</subject><issn>1065-9471</issn><issn>1097-0193</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1ks1u1TAQhSMEoj-w4AWQJTZ0kVvbiROHBVKpKEUqYgNiaTmOk7hK7GA7rS6rPgISz8CL9UmY9N4WikBexDr55ozPaJLkGcErgjE97OtxRRnLigfJLsFVmWJSZQ-Xe8HSKi_JTrIXwjnGhDBMHic7WU6gsGS7yc-T2aponL2--hGin1WcvUbKzdNgbPcKfelN1GiUMWqP2i0rB1A6q6NRyOsAglUaGdCgBvXrSfvrq-8S2Au58EiG4JSRUQd0aWKPbjuBkbFRd97ENTg18419ABEF1Ztvbuq9tkY-SR61cgj66fa7n3w-efvp-DQ9-_ju_fHRWaoYZE1bSbOaMUhdVwUleUVgEHnbFkTVRS0xoZzKjDS8qCnPJS_LvCoUV03ZKIoJzvaT1xvfaa5H3ShtI7xRTB6y-bVw0oj7f6zpRecuBKecY87A4OXWwLuvsw5RjCYoPQzSajcHQVlWAVmUFNAXf6HnbvYw24VilDNOSv6b6uSghbGtg75qMRVHJWSGSJgAtfoHBafRo1HO6taAfq_gYFOgvAvB6_YuI8Fi2SkBOyVudgrY538O5Y68XSIADjfAJXRZ_99JnL75sLH8BXVM23Y</recordid><startdate>20210815</startdate><enddate>20210815</enddate><creator>Jiang, Yuchao</creator><creator>Duan, Mingjun</creator><creator>Li, Xiangkui</creator><creator>Huang, Huan</creator><creator>Zhao, Guocheng</creator><creator>Li, Xuan</creator><creator>Li, Shicai</creator><creator>Song, Xufeng</creator><creator>He, Hui</creator><creator>Yao, Dezhong</creator><creator>Luo, Cheng</creator><general>John Wiley & Sons, Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7012-0559</orcidid><orcidid>https://orcid.org/0000-0003-0524-5886</orcidid></search><sort><creationdate>20210815</creationdate><title>Function–structure coupling: White matter functional magnetic resonance imaging hyper‐activation associates with structural integrity reductions in schizophrenia</title><author>Jiang, Yuchao ; Duan, Mingjun ; Li, Xiangkui ; Huang, Huan ; Zhao, Guocheng ; Li, Xuan ; Li, Shicai ; Song, Xufeng ; He, Hui ; Yao, Dezhong ; Luo, Cheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5106-fa23b55065b96214910194ff61cb6ba01282a31d86b284a877496c8cd7dc20103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>activation</topic><topic>Adult</topic><topic>Anisotropy</topic><topic>Brain</topic><topic>Brain mapping</topic><topic>Cognition</topic><topic>Couplings</topic><topic>Data processing</topic><topic>Diffusion Tensor Imaging</topic><topic>Emotional behavior</topic><topic>Emotions</topic><topic>Female</topic><topic>fMRI</topic><topic>frontal</topic><topic>Functional analysis</topic><topic>Functional magnetic resonance imaging</topic><topic>Functional Neuroimaging</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Medical imaging</topic><topic>Mental disorders</topic><topic>Middle Aged</topic><topic>Neuroimaging</topic><topic>Resonance</topic><topic>Schizophrenia</topic><topic>Schizophrenia - diagnostic imaging</topic><topic>Schizophrenia - pathology</topic><topic>Schizophrenia - physiopathology</topic><topic>Somatotropin</topic><topic>Structural integrity</topic><topic>Structure-function relationships</topic><topic>Substantia alba</topic><topic>Tensors</topic><topic>Time series</topic><topic>white matter</topic><topic>White Matter - diagnostic imaging</topic><topic>White Matter - pathology</topic><topic>White Matter - physiopathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Yuchao</creatorcontrib><creatorcontrib>Duan, Mingjun</creatorcontrib><creatorcontrib>Li, Xiangkui</creatorcontrib><creatorcontrib>Huang, Huan</creatorcontrib><creatorcontrib>Zhao, Guocheng</creatorcontrib><creatorcontrib>Li, Xuan</creatorcontrib><creatorcontrib>Li, Shicai</creatorcontrib><creatorcontrib>Song, Xufeng</creatorcontrib><creatorcontrib>He, Hui</creatorcontrib><creatorcontrib>Yao, Dezhong</creatorcontrib><creatorcontrib>Luo, Cheng</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human brain mapping</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Yuchao</au><au>Duan, Mingjun</au><au>Li, Xiangkui</au><au>Huang, Huan</au><au>Zhao, Guocheng</au><au>Li, Xuan</au><au>Li, Shicai</au><au>Song, Xufeng</au><au>He, Hui</au><au>Yao, Dezhong</au><au>Luo, Cheng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Function–structure coupling: White matter functional magnetic resonance imaging hyper‐activation associates with structural integrity reductions in schizophrenia</atitle><jtitle>Human brain mapping</jtitle><addtitle>Hum Brain Mapp</addtitle><date>2021-08-15</date><risdate>2021</risdate><volume>42</volume><issue>12</issue><spage>4022</spage><epage>4034</epage><pages>4022-4034</pages><issn>1065-9471</issn><eissn>1097-0193</eissn><abstract>White matter (WM) microstructure deficit may be an underlying factor in the brain dysconnectivity hypothesis of schizophrenia using diffusion tensor imaging (DTI). However, WM dysfunction is unclear in schizophrenia. This study aimed to investigate the association between structural deficits and functional disturbances in major WM tracts in schizophrenia. Using functional magnetic resonance imaging (fMRI) and DTI, we developed the skeleton‐based WM functional analysis, which could achieve voxel‐wise function–structure coupling by projecting the fMRI signals onto a skeleton in WM. We measured the fractional anisotropy (FA) and WM low‐frequency oscillation (LFO) and their couplings in 93 schizophrenia patients and 122 healthy controls (HCs). An independent open database (62 schizophrenia patients and 71 HCs) was used to test the reproducibility. Finally, associations between WM LFO and five behaviour assessment categories (cognition, emotion, motor, personality and sensory) were examined. This study revealed a reversed pattern of structure and function in frontotemporal tracts, as follows. (a) WM hyper‐LFO was associated with reduced FA in schizophrenia. (b) The function–structure association was positive in HCs but negative in schizophrenia patients. Furthermore, function–structure dissociation was exacerbated by long illness duration and severe negative symptoms. (c) WM activations were significantly related to cognition and emotion. This study indicated function–structure dys‐coupling, with higher LFO and reduced structural integration in frontotemporal WM, which may reflect a potential mechanism in WM neuropathologic processing of schizophrenia.
Hyper‐activation of white matter associates with loss of white matter integrity in patients with schizophrenia. The function–structure dys‐coupling exacerbated with long illness duration and severe negative symptoms in schizophrenia, and also associated with cognition and emotion.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>34110075</pmid><doi>10.1002/hbm.25536</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-7012-0559</orcidid><orcidid>https://orcid.org/0000-0003-0524-5886</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | activation Adult Anisotropy Brain Brain mapping Cognition Couplings Data processing Diffusion Tensor Imaging Emotional behavior Emotions Female fMRI frontal Functional analysis Functional magnetic resonance imaging Functional Neuroimaging Humans Magnetic Resonance Imaging Male Medical imaging Mental disorders Middle Aged Neuroimaging Resonance Schizophrenia Schizophrenia - diagnostic imaging Schizophrenia - pathology Schizophrenia - physiopathology Somatotropin Structural integrity Structure-function relationships Substantia alba Tensors Time series white matter White Matter - diagnostic imaging White Matter - pathology White Matter - physiopathology |
title | Function–structure coupling: White matter functional magnetic resonance imaging hyper‐activation associates with structural integrity reductions in schizophrenia |
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