Spontaneous low-frequency fluctuations in the neural system for emotional perception in major psychiatric disorders: amplitude similarities and differences across frequency bands

Spontaneous low-frequency fluctuations in the neural system for emotional perception in major psychiatric disorders: amplitude similarities and differences across frequency bands

J Psychiatry Neurosci 2019;44(2):132-141 | PDF | Appendix

Miao Chang, PhD; Elliot K. Edmiston, PhD; Fay Y. Womer, MD, PhD; Qian Zhou, PhD; Shengnan Wei, PhD; Xiaowei Jiang, MD; Yifang Zhou, MD; Yuting Ye, PhD; Haiyan Huang, PhD; Xi-Nian Zuo, PhD; Ke Xu, MD, PhD; Yanqing Tang, MD, PhD*; Fei Wang, MD, PhD*

Abstract

Background: Growing evidence indicates both shared and distinct features of emotional perception in schizophrenia, bipolar disorder and major depressive disorder. In these disorders, alterations in spontaneous low-frequency fluctuations have been reported in the neural system for emotional perception, but the similarities and differences in the amplitude of low-frequency fluctuation (ALFF) across the 3 disorders are unknown.

Methods: We compared ALFF and its signal balance in the neural system for emotional perception at 2 frequency bands (slow-5 and slow-4) in 119 participants with schizophrenia, 100 with bipolar disorder, 123 with major depressive disorder and 183 healthy controls. We performed exploratory Pearson partial correlation analyses to determine the relationship between ALFF signal balance and clinical variables.

Results: We observed commonalities in ALFF change patterns across the 3 disorders for emotional perception neural substrates, such as increased ALFF in the anterior cerebrum (including subcortical, limbic, paralimbic and heteromodal cortical regions) and decreased ALFF in the posterior visual cortices. Schizophrenia, bipolar disorder and major depressive disorder showed significantly decreased ALFF signal balance in the neural system for emotional perception at both slow-5 and slow-4 frequency bands, with the greatest alterations for schizophrenia, followed by bipolar disorder and major depressive disorder. We found a negative correlation between ALFF signal balance and negative/disorganized symptoms in slow-4 across the 3 disorders.

Limitations: The relatively broad age range in our sample and the cross-sectional study design may not account for our findings.

Conclusion: The extent of the commonalities we observed further support the concept of core neurobiological disruptions shared among the 3 disorders; ALFF signal balance could be an important neuroimaging marker for the diagnosis and treatment of schizophrenia, bipolar disorder and major depressive disorder.


Submitted Nov. 9, 2017; Revised Apr. 22, 2018; Accepted May 29, 2018; Published online Nov. 28, 2018

Acknowledgements: The authors thank all the participants for their cooperation and are grateful for the support of Shenyang Mental Health Centre, Department of Psychiatry and Radiology, First Affiliated Hospital of China Medical University. The authors were supported by research grants from the National Natural Science Foundation of China (81571311, 81071099 and 81271499 to Y. Tang; 81725005, 81571331 to F. Wang), the National Science Fund for Distinguished Young Scholars (81725005 to F. Wang), the National Key Research and Development Program (2016YFC1306900 to Y. Tang), the Liaoning Education Foundation (Pandeng Scholar, F. Wang), the National Key Research and Development Program (2016YFC0904300 to F. Wang) and the National High Tech Development Plan (863; 2015AA020513 to F. Wang).

Affiliations: From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).

Competing interests: None declared.

Contributors: F. Wang designed the study. X. Jiang, Y. Tang, S. Wei, F. Womer, K. Xu, Q. Zhou and Y. Zhou acquired the data, which H. Huang, Y. Ye and X. Zuo analyzed. M. Chang and E. Edmiston wrote the article, which all authors reviewed. All authors approved the final version to be published and can certify that no other individuals not listed as authors have made substantial contributions to the paper.

DOI: 10.1503/jpn.170226

Correspondence to: F. Wang, Department of Psychiatry and Radiology, First Affiliated Hospital, China Medical University, 155 Nanjing North Street, Heping District, Shenyang, Liaoning 110001, PR China; fei.wang@cmu.edu.cn; Y. Tang, Department of Psychiatry and Geriatrics, First Affiliated Hospital, China Medical University, 155 Nanjing North Street, Heping District, Shenyang, Liaoning 110001, PR China; yanqingtang@163.com.