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Deficit in parietal memory network underlies auditory hallucination: a longitudinal study

Qian Guo, Yang Hu, Botao Zeng, Yingying Tang, Tianhong Zhang, Jinhong Wang, Georg Northoff, Chunbo Li, Donald Goff, Jijun Wang, Zhi Yang
doi: https://doi.org/10.1101/204008
Qian Guo
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaBrain Science and Technology Research Center, Shanghai Jiao Tong University, Shanghai, China
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Yang Hu
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
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Botao Zeng
Department of Psychiatry, Qingdao Mental Health Center, Qingdao, China
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Yingying Tang
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
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Tianhong Zhang
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
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Jinhong Wang
Department of Medical Imaging, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
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Georg Northoff
Mind, Brain Imaging, and Neuroethics, Royal’s Institute of Mental Health Research, University of Ottawa, Ottawa, ON, Canada
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Chunbo Li
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaBrain Science and Technology Research Center, Shanghai Jiao Tong University, Shanghai, ChinaKey Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Bio-X Institutes, Ministry of Education, Shanghai Jiao Tong University, Shanghai, China
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Donald Goff
Department of Psychiatry, NYU Langone Medical Center, New York, USA
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Jijun Wang
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaBrain Science and Technology Research Center, Shanghai Jiao Tong University, Shanghai, ChinaKey Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Bio-X Institutes, Ministry of Education, Shanghai Jiao Tong University, Shanghai, China
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Zhi Yang
Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaBrain Science and Technology Research Center, Shanghai Jiao Tong University, Shanghai, China
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  • For correspondence: yangz@psych.ac.cn
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Abstract

Auditory hallucination is a prominent and common symptom in schizophrenia. Previous neuroimaging studies have yielded mixed results of its brain network deficits. We proposed a novel hypothesis that parietal memory network, centered at the precuneus, plays a critical role in auditory hallucination. This network is adjacent and partially overlaps with the default mode network, and has been associated with brain function of familiarity labelling in memory processing. Using a longitudinal design and a large cohort of first-episode, drug-naïve schizophrenia patients, we examined this hypothesis and further investigated whether the functional connectivity patterns of the parietal memory network can serve as a neuroimaging marker for auditory hallucination and help to predict future treatment effects. Resting-state scans from 59 first-episode drug-naïve schizophrenic patients (27 with and 32 without hallucination) and 53 healthy control subjects were acquired at the baseline test, and 56 of them were scanned again after two months. Functional connectivity strength within the parietal memory network and between this network and memory hubs was across the three groups at baseline and follow-up scans. Results showed that decreased functional connectivity strength within the parietal memory network was specific to the auditory hallucination group (p = 0.009, compare to the healthy subjects; p = 0.029, compare to the patients without hallucination), with the precuneus representing the largest group difference. The intra-network connectivity strength of the precuneus negatively correlated with the severity of hallucination at the baseline scan (r = −0.437, p = 0.029), and it was significantly increased after two-month medication (p = 0.039). Logistic regression analysis and crossvalidation test demonstrated that the functional connectivity strength of the precuneus and precuneus-hippocampus connectivity could differentiate patients with or without auditory hallucination with a sensitivity of 0.750 and a specificity of 0.708. Moreover, crossvalidation test showed that these imaging features at the baseline scan well predicted the extents of positive symptom improvement in the hallucination group after the two-month medication (R2 = 0.433, p = 0.022). Our results provide evidence for a critical role of the parietal memory network underlying auditory hallucination, and further propose a novel neuroimaging marker for identifying patients, accessing severity, and prognosis of treatment effect for auditory hallucination.

AH
auditory hallucination
AHRS
Auditory Hallucination Rating Scale
AUC
Area-under-curve
BPRS
Brief Psychiatric Rating Scale
DMN
default mode network
DSM-IV
Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition
DUP
duration of untreated psychosis
FCS
functional connectivity strength
HC
healthy control
IC
independent component
PMN
parietal memory network
NMDA
N-methyl-D-aspartate
RSN
resting state network
rs-fMRI
resting-state functional MRI
rTMS
repetitive transcranial magnetic stimulation
SANS
Expanded Version and the Scale for Assessment of Negative Symptoms
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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 16, 2017.
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Deficit in parietal memory network underlies auditory hallucination: a longitudinal study
Qian Guo, Yang Hu, Botao Zeng, Yingying Tang, Tianhong Zhang, Jinhong Wang, Georg Northoff, Chunbo Li, Donald Goff, Jijun Wang, Zhi Yang
bioRxiv 204008; doi: https://doi.org/10.1101/204008
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Deficit in parietal memory network underlies auditory hallucination: a longitudinal study
Qian Guo, Yang Hu, Botao Zeng, Yingying Tang, Tianhong Zhang, Jinhong Wang, Georg Northoff, Chunbo Li, Donald Goff, Jijun Wang, Zhi Yang
bioRxiv 204008; doi: https://doi.org/10.1101/204008

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