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Characteristics of disrupted topological organization in white matter functional connectome in schizophrenia

Published online by Cambridge University Press:  03 September 2020

Yuchao Jiang Open the ORCID record for Yuchao Jiang [Opens in a new window] ,
Dezhong Yao ,
Jingyu Zhou ,
Yue Tan ,
Huan Huang ,
MeiLin Wang ,
Xin Chang ,
Mingjun Duan  and
Cheng Luo
Yuchao Jiang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China
Dezhong Yao
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China Research Unit of NeuroInformation, Chinese Academy of Medical Sciences, 2019RU035, Chengdu, P. R. China School of Electrical Engineering, Zhengzhou University, Zhengzhou, P. R. China
Jingyu Zhou
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China
Yue Tan
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China
Huan Huang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China
MeiLin Wang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China
Xin Chang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China
Mingjun Duan
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China Department of Psychiatry, Chengdu Mental Health Center, Chengdu, P. R. China
Cheng Luo*
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China Research Unit of NeuroInformation, Chinese Academy of Medical Sciences, 2019RU035, Chengdu, P. R. China
*
Author for correspondence: Cheng Luo, E-mail: chengluo@uestc.edu.cn
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Abstract

Background

Neuroimaging characteristics have demonstrated disrupted functional organization in schizophrenia (SZ), involving large-scale networks within grey matter (GM). However, previous studies have ignored the role of white matter (WM) in supporting brain function.

Methods

Using resting-state functional MRI and graph theoretical approaches, we investigated global topological disruptions of large-scale WM and GM networks in 93 SZ patients and 122 controls. Six global properties [clustering coefficient (Cp), shortest path length (Lp), local efficiency (Eloc), small-worldness (σ), hierarchy (β) and synchronization (S) and three nodal metrics [nodal degree (Knodal), nodal efficiency (Enodal) and nodal betweenness (Bnodal)] were utilized to quantify the topological organization in both WM and GM networks.

Results

At the network level, both WM and GM networks exhibited reductions in Eloc, Cp and S in SZ. The SZ group showed reduced σ and β only for the WM network. Furthermore, the Cp, Eloc and S of the WM network were negatively correlated with negative symptoms in SZ. At the nodal level, the SZ showed nodal disturbances in the corpus callosum, optic radiation, posterior corona radiata and tempo-occipital WM tracts. For GM, the SZ manifested increased nodal centralities in frontoparietal regions and decreased nodal centralities in temporal regions.

Conclusions

These findings provide the first evidence for abnormal global topological properties in SZ from the perspective of a substantial whole brain, including GM and WM. Nodal centralities enhance GM areas, along with a reduction in adjacent WM, suggest that WM functional alterations may be compensated for adjacent GM impairments in SZ.

Keywords

ConnectomefMRIgraph theoryschizophreniawhite matter
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 7 , May 2022 , pp. 1333 - 1343
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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