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Common and distinct global functional connectivity density alterations in patients with bipolar disorder with and without auditory verbal hallucination during major depressive episodes

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Abstract

Although an increasing number of studies has explored the neural mechanisms of auditory verbal hallucination (AVH) using many modalities, including neuroimaging, neurotransmitters, and electroencephalography, the etiology of AVH remains unclear. In this study, we investigated the neuroimaging characteristics of AVH in patients with bipolar disorder (BD) experiencing depressive episodes with and without AVH. For this study, we recruited 80 patients with BD and depressive status (40 with and 40 without AVH), and 40 healthy individuals. Their global functional connectivity density (gFCD) was screened by functional magnetic resonance imaging. Differences in gFCD among the three groups were tested using voxel-wise one-way analysis of covariance. Patients in both BD groups demonstrated increased gFCD in the central parietal lobe, insular lobe, and middle cingulate cortex, and decreased gFCD in the posterior parietal cortex, lateral prefrontal cortex, and occipital lobe (all bilateral). We defined these alterations as the common aberrant gFCD pattern for BD with and without AVH. Compared with the other two groups, patients in the BD with AVH group demonstrated increased gFCD in the Broca and Wernicke regions, and decreased gFCD in the hippocampus (all bilateral). We defined these alterations as the distinct aberrant gFCD pattern for BD with AVH. To our knowledge, this report is the first to date to describe gFCD alterations in patients with BD with and without AVH. Our findings suggest that disturbances in brain activity and information communication capacity in patients with BD and AVH are located mainly in the left frontoparietal network, control network, and memory circuit. However, these observations were made only in patients with BD during depressive episodes, and without consideration of many factors, such as the treatment mode, symptom relapse, and BD subtype. Hence, the conclusions of this study merely provide clues for further study, and do not fully represent brain alterations in patients with BD and AVH. Further large-sample cohort studies are needed to clarify and expand on these findings.

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (81871052 to C.Z., 81801679 and 81571319 to Y.X.), the Key Projects of the Natural Science Foundation of Tianjin, China (17JCZDJC35700 to C.Z.), the Tianjin Health Bureau Foundation (2014KR02 to C.Z.), Tianjin Anding Hospital Award 300000 Yuan to C.J., the National Key Research and Development Program of China (2016YFC1307004 to Y.X.), the Shanxi Science and Technology Innovation Training Team’s Multidisciplinary Team for Cognitive Impairment (201705D131027 to Y.X.), the Zhejiang Public Welfare Fund Project (LGF18H090002 to D.J), and the key project of the Wenzhou Science and Technology Bureau (ZS2017011 to X.L).

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Author notes

  1. Lixue Qiu

    Present address: Psychiatric-Neuroimaging-Genetics Laboratory, Wenzhou Seventh People’s Hospital, Wenzhou, 325000, Zhejiang Province, China

  2. Feng Ji

    Present address: School of Mental Health, Jining Medical University, Jining, 272119, Shandong Province, China

  3. Gang Li

    Present address: Department of Psychiatry, Tianshui Third Hospital, Tianshui, 741000, Gansu Province, China

Authors and Affiliations

  1. Psychiatric-Neuroimaging-Genetics Laboratory, Wenzhou Seventh People’s Hospital, Wenzhou, 325000, Zhejiang Province, China

    Jaen Ye, Deguo Jiang & Chuanjun Zhuo

  2. School of Mental Health, Jining Medical University, Jining, 272119, Shandong Province, China

    Gongying Li & Chuanjun Zhuo

  3. Psychiatric-Neuroimaging-Genetics-Comorbidity Laboratory, Tianjin Mental Health Centre, Mental Health Teaching Hospital of Tianjin Medical University, Tianjin Anding Hospital, Tianjin, 300222, China

    Xiaoyan Ma, Ranli Li, Hongjun Tian, Lina Wang, Guangdong Chen & Chuanjun Zhuo

  4. Department of Psychiatry, First Hospital/First Clinical Medical College of Shanxi Medical University, Taiyuan, China

    Yong Xu & Chuanjun Zhuo

  5. MDT Center for Cognitive Impairment and Sleep Disorders, First Hospital of Shanxi Medical University, Taiyuan, 030001, China

    Yong Xu & Chuanjun Zhuo

  6. Co-collaboration Laboratory of China and Canada, Xiamen Xianyue Hospital and University of Alberta, Xiamen, 361000, China

    Wenqiang Wang & Chuanjun Zhuo

  7. Department of Psychiatry, Wenzhou Kangning Hospital, Wenzhou Medical University Affiliated Wenzhou kangning Hospital, Zhejiang Province, 325002, China

    Jianshe Pan

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  1. Lixue Qiu
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Correspondence to Chuanjun Zhuo.

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The authors declare that they have no conflict of interest.

Ethical approval

The Ethics Committee of Wenzhou Seventh People’s Hospital approved this study (No. ZS2017011). All procedures performed in studies involving human participants were in accordance with the ethics standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethics standards.

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Written informed consent was obtained from all participants or their legal guardians included in the study.

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Lixue Qiu, Jaen Ye, Feng Ji, and Gang Li are the co-first authors for this work.

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Qiu, L., Ye, J., Ji, F. et al. Common and distinct global functional connectivity density alterations in patients with bipolar disorder with and without auditory verbal hallucination during major depressive episodes. Brain Imaging and Behavior 14, 2724–2730 (2020). https://doi.org/10.1007/s11682-019-00222-4

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