Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations

Purpose: Auditory hallucinations (AH), typically hearing voices, are a core symptom in schizophrenia. They may result from deficits in dynamic functional connectivity (FC) between cortical regions supporting speech production and language perception that interfere with the ability to recognize self-...

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Main Authors: Wenjing Zhang, Siyi Li, Xiuli Wang, Yao Gong, Li Yao, Yuan Xiao, Jieke Liu, Sarah K. Keedy, Qiyong Gong, John A. Sweeney, Su Lui
Format: Article
Language:English
Published: Elsevier 2018-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158218302018
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author Wenjing Zhang
Siyi Li
Xiuli Wang
Yao Gong
Li Yao
Yuan Xiao
Jieke Liu
Sarah K. Keedy
Qiyong Gong
John A. Sweeney
Su Lui
author_facet Wenjing Zhang
Siyi Li
Xiuli Wang
Yao Gong
Li Yao
Yuan Xiao
Jieke Liu
Sarah K. Keedy
Qiyong Gong
John A. Sweeney
Su Lui
author_sort Wenjing Zhang
collection DOAJ
description Purpose: Auditory hallucinations (AH), typically hearing voices, are a core symptom in schizophrenia. They may result from deficits in dynamic functional connectivity (FC) between cortical regions supporting speech production and language perception that interfere with the ability to recognize self-generated speech as not coming from external sources. We tested this hypothesis by investigating dynamic connectivity between the frontal cortex region related to language production and the temporal cortex region related to auditory processing. Methods: Resting-state fMRI scans were acquired from 18 schizophrenia patients with AH (AH+), 17 schizophrenia patients without AH (AH-) and 22 healthy controls. A multiband sequence with TR = 427 ms was adopted to provide relatively high temporal resolution data for characterizing dynamic FC. Analysis focused on connectivity between speech production and language comprehension areas, eloquent language cortex in the left hemisphere. Two frequency bands of brain oscillatory activity were evaluated (0.01–0.027 Hz, 0.027–0.08 Hz) in which differential alterations that have been previously linked to schizophrenia. Conventional static FC maps of these seeds were also calculated. Results: Dynamic connectivity analysis indicated that AH+ patients showed not only less temporal variability but transient lower strength in connectivity between speech and auditory areas than healthy controls, while AH- patients not. These findings were restricted to 0.027–0.08 Hz activity. In static connectivity analysis, no significant differences were observed in connectivity between speech production and language comprehension areas in either frequency band. Conclusions: Reduced temporal variability and connectivity strength between key regions of eloquent language cortex may represent a mechanism for AH in schizophrenia. Keywords: Schizophrenia, Auditory hallucinations, Dynamic, Functional connectivity, Language areas, Multiband
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spelling doaj.art-f6466d68d731489e9eb1ff51693c23282022-12-22T01:57:07ZengElsevierNeuroImage: Clinical2213-15822018-01-0119918924Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinationsWenjing Zhang0Siyi Li1Xiuli Wang2Yao Gong3Li Yao4Yuan Xiao5Jieke Liu6Sarah K. Keedy7Qiyong Gong8John A. Sweeney9Su Lui10Department of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, China; Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, ChinaDepartment of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, China; Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, ChinaThe Fourth People’s Hospital of Chengdu, Chengdu, ChinaThe Fourth People’s Hospital of Chengdu, Chengdu, ChinaDepartment of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, China; Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, ChinaDepartment of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, China; Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, ChinaDepartment of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, China; Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, ChinaDepartment of Psychiatry and Behavioral Neuroscience, University of Chicago, IL, USAHuaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, ChinaHuaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, China; Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, OH, USADepartment of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, China; Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, China; Department of Radiology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, China; Corresponding author at: Department of Radiology, The Center for Medical Imaging, West China Hospital of Sichuan University, No. 37 Guoxue Alley, Chengdu 610041, China.Purpose: Auditory hallucinations (AH), typically hearing voices, are a core symptom in schizophrenia. They may result from deficits in dynamic functional connectivity (FC) between cortical regions supporting speech production and language perception that interfere with the ability to recognize self-generated speech as not coming from external sources. We tested this hypothesis by investigating dynamic connectivity between the frontal cortex region related to language production and the temporal cortex region related to auditory processing. Methods: Resting-state fMRI scans were acquired from 18 schizophrenia patients with AH (AH+), 17 schizophrenia patients without AH (AH-) and 22 healthy controls. A multiband sequence with TR = 427 ms was adopted to provide relatively high temporal resolution data for characterizing dynamic FC. Analysis focused on connectivity between speech production and language comprehension areas, eloquent language cortex in the left hemisphere. Two frequency bands of brain oscillatory activity were evaluated (0.01–0.027 Hz, 0.027–0.08 Hz) in which differential alterations that have been previously linked to schizophrenia. Conventional static FC maps of these seeds were also calculated. Results: Dynamic connectivity analysis indicated that AH+ patients showed not only less temporal variability but transient lower strength in connectivity between speech and auditory areas than healthy controls, while AH- patients not. These findings were restricted to 0.027–0.08 Hz activity. In static connectivity analysis, no significant differences were observed in connectivity between speech production and language comprehension areas in either frequency band. Conclusions: Reduced temporal variability and connectivity strength between key regions of eloquent language cortex may represent a mechanism for AH in schizophrenia. Keywords: Schizophrenia, Auditory hallucinations, Dynamic, Functional connectivity, Language areas, Multibandhttp://www.sciencedirect.com/science/article/pii/S2213158218302018
spellingShingle Wenjing Zhang
Siyi Li
Xiuli Wang
Yao Gong
Li Yao
Yuan Xiao
Jieke Liu
Sarah K. Keedy
Qiyong Gong
John A. Sweeney
Su Lui
Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
NeuroImage: Clinical
title Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
title_full Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
title_fullStr Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
title_full_unstemmed Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
title_short Abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
title_sort abnormal dynamic functional connectivity between speech and auditory areas in schizophrenia patients with auditory hallucinations
url http://www.sciencedirect.com/science/article/pii/S2213158218302018
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