Abnormal dynamic resting-state brain network organization in auditory verbal hallucination

Haiyang Geng,Yue-Jia Luo,Pengfei Xu,Iris E Sommer,Branislava Ćurčić-Blake,André Aleman

doi:10.1007/s00429-020-02119-1

Abstract

Auditory-verbal hallucinations (AVH) are a key symptom of schizophrenia. Recent neuroimaging studies examining dynamic functional connectivity suggest that disrupted dynamic interactions between brain networks characterize complex symptoms in mental illness including schizophrenia. Studying dynamic connectivity may be especially relevant for hallucinations, given their fluctuating phenomenology. Indeed, it remains unknown whether AVH in schizophrenia are directly related to altered dynamic connectivity within and between key brain networks involved in auditory perception and language, emotion processing, and top-down control. In this study, we used dynamic connectivity approaches including sliding window and k-means to examine dynamic interactions among brain networks in schizophrenia patients with and without a recent history of AVH. Dynamic brain network analysis revealed that patients with AVH spent less time in a ‘network-antagonistic’ brain state where the default mode network (DMN) and the language network were anti-correlated, and had lower probability to switch into this brain state. Moreover, patients with AVH showed a lower connectivity within the language network and the auditory network, and lower connectivity was observed between the executive control and the language networks in certain dynamic states. Our study provides the first neuroimaging evidence of altered dynamic brain networks for understanding neural mechanisms of AVH in schizophrenia. The findings may inform and further strengthen cognitive models of AVH that aid the development of new coping strategies for patients.

Highlights

Auditory-verbal hallucinations (AVH) are perceptual experiences in the absence of external auditory-verbal stimuli, which are sufficiently compelling to be considered as true perceptions
The results showed that the main effects of TRs were not significant (all F (2, 35) < 2.26, all p > 0.12), which default mode network, LANG language network, AUD auditory network, *P < 0.05 suggested that different TRs did not significantly affect these measurements in dynamic analysis
The results showed that using these different window lengths can replicate our main findings including dynamic brain state patterns, dwell times, and functional connectivity in dynamic states

Summary

Introduction

Auditory-verbal hallucinations (AVH) are perceptual experiences in the absence of external auditory-verbal stimuli, which are sufficiently compelling to be considered as true perceptions. In recent years, resting-state functional connectivity has been commonly used in functional Magnetic Resonance Imaging (fMRI) studies to characterize interactions between brain networks in schizophrenia patients. These studies reported evidence of extensive disruption of brain networks including corticothalamo, fronto-limbic, and fronto-temporal connectivity in patients (Sarpal et al 2015; Sheffield and Barch 2016; van den Heuvel et al 2016; Chang et al 2017), consistent with the hypothesis of schizophrenia as a disorder of brain disconnection (Stephan et al 2009). While there are studies looking into dynamic changes in interactions within and between brain networks in schizophrenia patients (Damaraju et al 2014; Du et al 2016; Su et al 2016), it is very relevant and significant to investigate such dynamic changes in AVH which have a fluctuating nature

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