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Dynamic structure–function coupling across three major psychiatric disorders

Published online by Cambridge University Press:  12 December 2023

Zhe Zhang
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China School of Physics, Hangzhou Normal University, Hangzhou, China Institute of Brain Science, School of Basic Medical Sciences, Hangzhou Normal University, Hangzhou, China
Wei Wei
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
Sujie Wang
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China
Mingli Li
Affiliation:
Mental Health Center and Psychiatric Laboratory, West China Hospital of Sichuan University, Chengdu, China
Xiaojing Li
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
Xiaoyu Li
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China
Qiang Wang
Affiliation:
Mental Health Center and Psychiatric Laboratory, West China Hospital of Sichuan University, Chengdu, China
Hua Yu
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
Yamin Zhang
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
Wanjun Guo
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
Xiaohong Ma
Affiliation:
Mental Health Center and Psychiatric Laboratory, West China Hospital of Sichuan University, Chengdu, China
Liansheng Zhao
Affiliation:
Mental Health Center and Psychiatric Laboratory, West China Hospital of Sichuan University, Chengdu, China
Wei Deng
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
Pak C Sham
Affiliation:
Department of Psychiatry, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China Centre for PanorOmic Sciences, The University of Hong Kong, Hong Kong SAR, China State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Hong Kong SAR, China
Yu Sun*
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Department of Neurology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China
Tao Li*
Affiliation:
Department of Biomedical Engineering, & Department of Neurobiology, Key Laboratory for Biomedical Engineering of Ministry of Education, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University, Hangzhou, China Translational Psychiatry Research Laboratory, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, China
*
Corresponding author: Yu Sun; Email: yusun@zju.edu.cn; Tao Li; Email: litaozjusc@zju.edu.cn
Corresponding author: Yu Sun; Email: yusun@zju.edu.cn; Tao Li; Email: litaozjusc@zju.edu.cn

Abstract

Background

Convergent evidence has suggested atypical relationships between brain structure and function in major psychiatric disorders, yet how the abnormal patterns coincide and/or differ across different disorders remains largely unknown. Here, we aim to investigate the common and/or unique dynamic structure–function coupling patterns across major depressive disorder (MDD), bipolar disorder (BD), and schizophrenia (SZ).

Methods

We quantified the dynamic structure–function coupling in 452 patients with psychiatric disorders (MDD/BD/SZ = 166/168/118) and 205 unaffected controls at three distinct brain network levels, such as global, meso-, and local levels. We also correlated dynamic structure–function coupling with the topological features of functional networks to examine how the structure–function relationship facilitates brain information communication over time.

Results

The dynamic structure–function coupling is preserved for the three disorders at the global network level. Similar abnormalities in the rich-club organization are found in two distinct functional configuration states at the meso-level and are associated with the disease severity of MDD, BD, and SZ. At the local level, shared and unique alterations are observed in the brain regions involving the visual, cognitive control, and default mode networks. In addition, the relationships between structure–function coupling and the topological features of functional networks are altered in a manner indicative of state specificity.

Conclusions

These findings suggest both transdiagnostic and illness-specific alterations in the dynamic structure–function relationship of large-scale brain networks across MDD, BD, and SZ, providing new insights and potential biomarkers into the neurodevelopmental basis underlying the behavioral and cognitive deficits observed in these disorders.

Type
Original Article
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

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