Multilayer network instability underlying persistent auditory verbal hallucinations in schizophrenia

Jinguang Li; Jingqi He; Honghong Ren; Zongchang Li; Xiaoqian Ma; Liu Yuan; Lijun Ouyang; Chunwang Li; Xiaogang Chen; Ying He; Jinsong Tang

doi:10.1016/j.psychres.2024.116351

Multilayer network instability underlying persistent auditory verbal hallucinations in schizophrenia

Psychiatry Res. 2024 Dec 31:344:116351. doi: 10.1016/j.psychres.2024.116351. Online ahead of print.

Authors

Jinguang Li¹, Jingqi He², Honghong Ren³, Zongchang Li⁴, Xiaoqian Ma⁴, Liu Yuan⁴, Lijun Ouyang⁴, Chunwang Li⁵, Xiaogang Chen⁴, Ying He⁶, Jinsong Tang⁷

Affiliations

¹ Department of Psychiatry, National Clinical Research Center for Mental Disorders, and National Center for Mental Disorders, The Second Xiangya Hospital of Central South University, Changsha, Hunan, PR China; Department of Psychiatry, Wuhan Mental Health Center, Wuhan, PR China.
² Department of Psychiatry, Sir Run-Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, PR China.
³ Department of Psychiatry, National Clinical Research Center for Mental Disorders, and National Center for Mental Disorders, The Second Xiangya Hospital of Central South University, Changsha, Hunan, PR China; Shandong Provincial Hospital Affiliated to Shandong First Medical University, Shandong, PR China.
⁴ Department of Psychiatry, National Clinical Research Center for Mental Disorders, and National Center for Mental Disorders, The Second Xiangya Hospital of Central South University, Changsha, Hunan, PR China.
⁵ Department of Radiology, Hunan Children's Hospital, Changsha, Hunan, PR China.
⁶ Department of Psychiatry, National Clinical Research Center for Mental Disorders, and National Center for Mental Disorders, The Second Xiangya Hospital of Central South University, Changsha, Hunan, PR China. Electronic address: [email protected].
⁷ Department of Psychiatry, Sir Run-Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, PR China. Electronic address: [email protected].

PMID: 39787739
DOI: 10.1016/j.psychres.2024.116351

Abstract

Background: Auditory verbal hallucinations (AVHs) in schizophrenia (SCZ) are linked to brain network abnormalities. Resting-state fMRI studies often assume stable networks during scans, yet dynamic changes related to AVHs are not well understood.

Methods: We analyzed resting-state fMRI data from 60 SCZ patients with persistent AVHs (p-AVHs), 39 SCZ patients without AVHs (n-AVHs), and 59 healthy controls (HCs), matched for demographics. Using graph theory, we constructed a time-varying modular structure of brain networks, focusing on multilayer modularity. Network switching rates at global, subnetwork, and nodal levels were compared across groups and related to AVH severity.

Results: SCZ groups had higher switching rates in the subcortical network compared to HCs. Increased switching was found in two thalamic nodes for both patient groups. The p-AVH group showed lower switching rates in the default mode network (DMN) and two superior frontal gyrus nodes compared to HC and n-AVH groups. DMN switching rates negatively correlated with AVH severity in the p-AVH group.

Conclusions: Dynamic changes in brain networks, especially lower DMN and frontal region switching rates, may contribute to the development and persistence of AVHs in SCZ.

Keywords: Auditory verbal hallucinations; Default mode network; Multilayer network; Schizophrenia; Switching rate.