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Dynamic aberrances of substantia nigra-relevant coactivation patterns in first-episode treatment-naïve patients with schizophrenia

Published online by Cambridge University Press:  25 March 2024

Lihong Deng Open the ORCID record for Lihong Deng [Opens in a new window] ,
Wei Wei ,
Chunxia Qiao ,
Yubing Yin ,
Xiaojing Li ,
Hua Yu ,
Lingqi Jian ,
Xiaohong Ma ,
Liansheng Zhao  and
Qiang Wang
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Lihong Deng
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Wei Wei
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China
Chunxia Qiao
Affiliation:
Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Yubing Yin
Affiliation:
Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Xiaojing Li
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China
Hua Yu
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China
Lingqi Jian
Affiliation:
Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Xiaohong Ma
Affiliation:
Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Liansheng Zhao
Affiliation:
Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Qiang Wang
Affiliation:
Mental Health Center and Psychiatric Laboratory, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China
Wei Deng
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China
Wanjun Guo
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China
Tao Li*
Affiliation:
Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China Nanhu Brain-computer Interface Institute, Hangzhou, Zhejiang, China Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence, Zhejiang University, Hangzhou, Zhejiang, China NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou, Zhejiang, China
*
Corresponding author: Tao Li; Email: litaozjusc@zju.edu.cn
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Abstract

Background

Although dopaminergic disturbances are well-known in schizophrenia, the understanding of dopamine-related brain dynamics remains limited. This study investigates the dynamic coactivation patterns (CAPs) associated with the substantia nigra (SN), a key dopaminergic nucleus, in first-episode treatment-naïve patients with schizophrenia (FES).

Methods

Resting-state fMRI data were collected from 84 FES and 94 healthy controls (HCs). Frame-wise clustering was implemented to generate CAPs related to SN activation or deactivation. Connectome features of each CAP were derived using an edge-centric method. The occurrence for each CAP and the balance ratio for antagonistic CAPs were calculated and compared between two groups, and correlations between temporal dynamic metrics and symptom burdens were explored.

Results

Functional reconfigurations in CAPs exhibited significant differences between the activation and deactivation states of SN. During SN activation, FES more frequently recruited a CAP characterized by activated default network, language network, control network, and the caudate, compared to HCs (F = 8.54, FDR-p = 0.030). Moreover, FES displayed a tilted balance towards a CAP featuring SN-coactivation with the control network, caudate, and thalamus, as opposed to its antagonistic CAP (F = 7.48, FDR-p = 0.030). During SN deactivation, FES exhibited increased recruitment of a CAP with activated visual and dorsal attention networks but decreased recruitment of its opposing CAP (F = 6.58, FDR-p = 0.034).

Conclusion

Our results suggest that neuroregulatory dysfunction in dopaminergic pathways involving SN potentially mediates aberrant time-varying functional reorganizations in schizophrenia. This finding enriches the dopamine hypothesis of schizophrenia from the perspective of brain dynamics.

Keywords

brain dynamicscoactivation patterndopamine hypothesisedge-centric modelfirst-episode treatment-naïve schizophreniaresting-state fMRI
Type
Original Article
Information
Psychological Medicine , First View , pp. 1 - 11
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Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

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