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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Veröffentlicht in:Human brain mapping 2021-08, Vol.42 (12), p.4022-4034
Hauptverfasser: Jiang, Yuchao, Duan, Mingjun, Li, Xiangkui, Huang, Huan, Zhao, Guocheng, Li, Xuan, Li, Shicai, Song, Xufeng, He, Hui, Yao, Dezhong, Luo, Cheng
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container_end_page 4034
container_issue 12
container_start_page 4022
container_title Human brain mapping
container_volume 42
creator Jiang, Yuchao
Duan, Mingjun
Li, Xiangkui
Huang, Huan
Zhao, Guocheng
Li, Xuan
Li, Shicai
Song, Xufeng
He, Hui
Yao, Dezhong
Luo, Cheng
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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(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. 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Human Brain Mapping published by Wiley Periodicals LLC.</rights><rights>COPYRIGHT 2021 John Wiley &amp; 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). 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(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. 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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. 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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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