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Psychoradiological patterns of small-world properties and a systematic review of connectome studies of patients with 6 major psychiatric disorders

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J Psychiatry Neurosci 2018;43(6):416-427

Xueling Suo, MM;* Du Lei, PhD;* Lei Li, PhD;* Wenbin Li, MM; Jing Dai, MD; Song Wang, PhD; Manxi He, MD; Hongyan Zhu, MD; Graham J. Kemp, DSc; Qiyong Gong, MD, PhD


Background: Brain connectome research based on graph theoretical analysis shows that small-world topological properties play an important role in the structural and functional alterations observed in patients with psychiatric disorders. However, the reported global topological alterations in small-world properties are controversial, are not consistently conceptualized according to agreed-upon criteria, and are not critically examined for consistent alterations in patients with each major psychiatric disorder.

Methods: Based on a comprehensive PubMed search, we systematically reviewed studies using noninvasive neuroimaging data and graph theoretical approaches for 6 major psychiatric disorders: schizophrenia, major depressive disorder (MDD), attention-deficit/hyperactivity disorder (ADHD), bipolar disorder (BD), obsessive–compulsive disorder (OCD) and posttraumatic stress disorder (PTSD). Here, we describe the main patterns of altered small-world properties and then systematically review the evidence for these alterations in the structural and functional connectome in patients with these disorders.

Results: We selected 40 studies of schizophrenia, 33 studies of MDD, 5 studies of ADHD, 5 studies of BD, 7 studies of OCD and 5 studies of PTSD. The following 4 patterns of altered small-world properties are defined from the perspectives of segregation and integration: “regularization,” “randomization,” “stronger small-worldization” and “weaker small-worldization.” Although more differences than similarities are noted in patients with these disorders, a prominent trend is the structural regularization versus functional randomization in patients with schizophrenia.

Limitations: Differences in demographic and clinical characteristics, preprocessing steps and analytical methods can produce contradictory results, increasing the difficulty of integrating results across different studies.

Conclusion: Four psychoradiological patterns of altered small-world properties are proposed. The analysis of altered small-world properties may provide novel insights into the pathophysiological mechanisms underlying psychiatric disorders from a connectomic perspective. In future connectome studies, the global network measures of both segregation and integration should be calculated to fully evaluate altered small-world properties in patients with a particular disease.

*These authors contributed equally to this work.

Submitted Oct. 25, 2017; Revised Jan. 7, 2018; Accepted Jan. 28, 2018; Published online June 28, 2018

Acknowledgements: This study was supported by the National Natural Science Foundation (Grant Nos. 81501452, 81621003, 81761128023, 81220108013, 81227002 and 81030027), the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT, grant IRT16R52) of China, the Changjiang Scholar Professorship Award (Award No. T2014190) of China, and the CMB Distinguished a Professorship Award (Award No. F510000/G16916411) administered by the Institute of International Education. D. Lei is supported by the Newton International Fellowship from the Royal Society, and X. Suo is supported by the Graduate Student’s Research and Innovation Fund of Sichuan University (No. 2018YJSY099).

Affiliations: From the Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, 610041 China (Suo, Lei, Li, Gong); the Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK (Lei); the Department of Psychoradiology, Chengdu Mental Health Center, Chengdu, Sichuan, China (Dai, Wang, He); the Laboratory of Stem Cell Biology, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Zhu); the Liverpool Magnetic Resonance Imaging Centre (LiMRIC) and Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, UK (Kemp); and the Department of Psychology, School of Public Administration, Sichuan University, Chengdu, Sichuan, China (Gong).

Competing interests: None declared.

Contributors: X. Suo, D. Lei, H. Zhu and Q. Gong designed the study. X. Suo, D. Lei, L. Li, W. Li, S. Wang and G. Kemp acquired the data, which X. Suo, D. Lei, L. Li, W. Li, J. Dai, S. Wang, M. He and G. Kemp analyzed. X. Suo, D. Lei, L. Li and G. Kemp 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.170214

Correspondence to: H. Zhu, Laboratory of Stem Cell Biology, State Key Laboratory of Biotherapy, West China Hospital of Sichuan University, Chengdu, China; hyzhu_hmrrc@126.com; Q. Gong, Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital, Sichuan University, No. 37 Guo Xue Xiang, Chengdu, Sichuan 610041, China; W88qiyonggong@hmrrc.org.cn