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      Reduced nucleus accumbens functional connectivity in reward network and default mode network in patients with recurrent major depressive disorder

      research-article
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      Translational Psychiatry
      Nature Publishing Group UK
      Depression, Diagnostic markers

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          Abstract

          The nucleus accumbens (NAc) is considered a hub of reward processing and a growing body of evidence has suggested its crucial role in the pathophysiology of major depressive disorder (MDD). However, inconsistent results have been reported by studies on reward network-focused resting-state functional MRI (rs-fMRI). In this study, we examined functional alterations of the NAc-based reward circuits in patients with MDD via meta- and mega-analysis. First, we performed a coordinated-based meta-analysis with a new SDM-PSI method for all up-to-date rs-fMRI studies that focused on the reward circuits of patients with MDD. Then, we tested the meta-analysis results in the REST-meta-MDD database which provided anonymous rs-fMRI data from 186 recurrent MDDs and 465 healthy controls. Decreased functional connectivity (FC) within the reward system in patients with recurrent MDD was the most robust finding in this study. We also found disrupted NAc FCs in the DMN in patients with recurrent MDD compared with healthy controls. Specifically, the combination of disrupted NAc FCs within the reward network could discriminate patients with recurrent MDD from healthy controls with an optimal accuracy of 74.7%. This study confirmed the critical role of decreased FC in the reward network in the neuropathology of MDD. Disrupted inter-network connectivity between the reward network and DMN may also have contributed to the neural mechanisms of MDD. These abnormalities have potential to serve as brain-based biomarkers for individual diagnosis to differentiate patients with recurrent MDD from healthy controls.

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          Most cited references73

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          Acute and Longer-Term Outcomes in Depressed Outpatients Requiring One or Several Treatment Steps: A STAR*D Report

          This report describes the participants and compares the acute and longer-term treatment outcomes associated with each of four successive steps in the Sequenced Treatment Alternatives to Relieve Depression (STAR*D) trial.
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            The reward circuit: linking primate anatomy and human imaging.

            Although cells in many brain regions respond to reward, the cortical-basal ganglia circuit is at the heart of the reward system. The key structures in this network are the anterior cingulate cortex, the orbital prefrontal cortex, the ventral striatum, the ventral pallidum, and the midbrain dopamine neurons. In addition, other structures, including the dorsal prefrontal cortex, amygdala, hippocampus, thalamus, and lateral habenular nucleus, and specific brainstem structures such as the pedunculopontine nucleus, and the raphe nucleus, are key components in regulating the reward circuit. Connectivity between these areas forms a complex neural network that mediates different aspects of reward processing. Advances in neuroimaging techniques allow better spatial and temporal resolution. These studies now demonstrate that human functional and structural imaging results map increasingly close to primate anatomy.
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              The cognitive control of emotion.

              The capacity to control emotion is important for human adaptation. Questions about the neural bases of emotion regulation have recently taken on new importance, as functional imaging studies in humans have permitted direct investigation of control strategies that draw upon higher cognitive processes difficult to study in nonhumans. Such studies have examined (1) controlling attention to, and (2) cognitively changing the meaning of, emotionally evocative stimuli. These two forms of emotion regulation depend upon interactions between prefrontal and cingulate control systems and cortical and subcortical emotion-generative systems. Taken together, the results suggest a functional architecture for the cognitive control of emotion that dovetails with findings from other human and nonhuman research on emotion.
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                Author and article information

                Contributors
                guowenbin76@csu.edu.cn
                Journal
                Transl Psychiatry
                Transl Psychiatry
                Translational Psychiatry
                Nature Publishing Group UK (London )
                2158-3188
                6 June 2022
                6 June 2022
                2022
                : 12
                : 236
                Affiliations
                [1 ]GRID grid.452708.c, ISNI 0000 0004 1803 0208, Department of Psychiatry, , and National Clinical Research Center for Mental Disorders, The Second Xiangya Hospital of Central South University, ; Changsha, China
                [2 ]GRID grid.454868.3, ISNI 0000 0004 1797 8574, CAS Key Laboratory of Behavioral Science, Institute of Psychology, ; Beijing, China
                [3 ]GRID grid.410726.6, ISNI 0000 0004 1797 8419, Department of Psychology, , University of Chinese Academy of Sciences, ; Beijing, China
                [4 ]GRID grid.9227.e, ISNI 0000000119573309, International Big-Data Center for Depression Research, Chinese Academy of Sciences, ; Beijing, China
                [5 ]GRID grid.452661.2, ISNI 0000 0004 1803 6319, Department of Rehabilitation Medicine, , The First Affiliated Hospital, College of Medicine, Zhejiang University, ; Hangzhou, Zhejiang China
                [6 ]GRID grid.443257.3, ISNI 0000 0001 0741 516X, Center for Cognitive Science of Language, Beijing Language and Culture University, ; Beijing, China
                [7 ]GRID grid.410726.6, ISNI 0000 0004 1797 8419, Sino-Danish College, University of Chinese Academy of Sciences, ; Beijing, China
                [8 ]GRID grid.484648.2, ISNI 0000 0004 0480 4559, Sino-Danish Center for Education and Research, ; Beijing, China
                [9 ]GRID grid.137628.9, ISNI 0000 0004 1936 8753, Department of Child and Adolescent Psychiatry, , NYU Grossman School of Medicine, ; New York, 31 NY USA
                [10 ]GRID grid.250263.0, ISNI 0000 0001 2189 4777, Nathan Kline Institute for Psychiatric Research, ; Orangeburg, NY USA
                [11 ]GRID grid.186775.a, ISNI 0000 0000 9490 772X, Anhui Medical University, ; Hefei, Anhui China
                [12 ]GRID grid.24696.3f, ISNI 0000 0004 0369 153X, Beijing Anding Hospital, Capital Medical University, ; Beijing, China
                [13 ]GRID grid.452206.7, ISNI 0000 0004 1758 417X, Department of Psychiatry, , The First Affiliated Hospital of Chongqing Medical University, ; Chongqing, China
                [14 ]GRID grid.412601.0, ISNI 0000 0004 1760 3828, The First Affiliated Hospital of Jinan University, ; Guangzhou, Guangdong China
                [15 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, ; Hangzhou, Zhejiang China
                [16 ]GRID grid.452661.2, ISNI 0000 0004 1803 6319, Department of Radiology, , The First Affiliated Hospital, College of Medicine, Zhejiang University, ; Hangzhou, Zhejiang China
                [17 ]GRID grid.414902.a, ISNI 0000 0004 1771 3912, Department of Psychiatry, , First Affiliated Hospital of Kunming Medical University, ; Kunming, Yunnan China
                [18 ]GRID grid.412636.4, ISNI 0000 0004 1757 9485, Department of Psychiatry, , First Affiliated Hospital, China Medical University, ; Shenyang, Liaoning China
                [19 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, Department of Psychiatry, , Shanghai Jiao Tong University School of Medicine, ; Shanghai, China
                [20 ]GRID grid.412901.f, ISNI 0000 0004 1770 1022, Huanxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, ; Chengdu, Sichuan China
                [21 ]GRID grid.412901.f, ISNI 0000 0004 1770 1022, Psychoradiology Research Unit of Chinese Academy of Medical Sciences, West China Hospital of Sichuan University, ; Chengdu, Sichuan China
                [22 ]GRID grid.263826.b, ISNI 0000 0004 1761 0489, Department of Psychosomatics and Psychiatry, , Zhongda Hospital, School of Medicine, Southeast University, ; Nanjing, Jiangsu China
                [23 ]GRID grid.412901.f, ISNI 0000 0004 1770 1022, Mental Health Center, West China Hospital, Sichuan University, ; Chengdu, Sichuan China
                [24 ]GRID grid.263761.7, ISNI 0000 0001 0198 0694, Department of Clinical Psychology, , Suzhou Psychiatric Hospital, The Affiliated Guangji Hospital of Soochow University, ; Suzhou, Jiangsu China
                [25 ]GRID grid.263906.8, ISNI 0000 0001 0362 4044, Faculty of Psychology, , Southwest University, ; Chongqing, China
                [26 ]GRID grid.460074.1, ISNI 0000 0004 1784 6600, Department of Diagnostics, , Affiliated Hospital, Hangzhou Normal University Medical School, ; Hangzhou, Zhejiang China
                [27 ]GRID grid.459847.3, ISNI 0000 0004 1798 0615, National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital) & Key Laboratory of Mental Health, Ministry of Health (Peking University), ; Beijing, China
                [28 ]GRID grid.478124.c, ISNI 0000 0004 1773 123X, Xi’an Central Hospital, ; Xi’an, Shaanxi China
                [29 ]GRID grid.452290.8, ISNI 0000 0004 1760 6316, Department of Neurology, , Affiliated ZhongDa Hospital of Southeast University, ; Nanjing, Jiangsu China
                [30 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Department of Psychiatry, , The Fourth Affiliated Hospital, College of Medicine, Zhejiang University, ; Yiwu, Zhejiang China
                [31 ]GRID grid.203458.8, ISNI 0000 0000 8653 0555, Institute of Neuroscience, Chongqing Medical University, ; Chongqing, China
                [32 ]GRID grid.203458.8, ISNI 0000 0000 8653 0555, Chongqing Key Laboratory of Neurobiology, ; Chongqing, China
                [33 ]GRID grid.452206.7, ISNI 0000 0004 1758 417X, Department of Neurology, , The First Affiliated Hospital of Chongqing Medical University, ; Chongqing, China
                [34 ]GRID grid.410595.c, ISNI 0000 0001 2230 9154, Center for Cognition and Brain Disorders, Institutes of Psychological Sciences, Hangzhou Normal University, ; Hangzhou, Zhejiang China
                [35 ]GRID grid.410595.c, ISNI 0000 0001 2230 9154, Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, ; Hangzhou, Zhejiang China
                [36 ]GRID grid.452438.c, ISNI 0000 0004 1760 8119, The First Affiliated Hospital of Xi’an Jiaotong University, ; Xi’an, Shaanxi China
                [37 ]GRID grid.452461.0, ISNI 0000 0004 1762 8478, First Hospital of Shanxi Medical University, ; Taiyuan, Shanxi China
                [38 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, Laboratory of Psychological Health and Imaging, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, ; Shanghai, China
                [39 ]GRID grid.20513.35, ISNI 0000 0004 1789 9964, State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, ; Beijing, China
                [40 ]GRID grid.454868.3, ISNI 0000 0004 1797 8574, Magnetic Resonance Imaging Research Center, Institute of Psychology, Chinese Academy of Sciences, ; Beijing, China
                Author information
                http://orcid.org/0000-0003-0903-7945
                http://orcid.org/0000-0002-8748-9085
                http://orcid.org/0000-0002-5912-4871
                http://orcid.org/0000-0001-5533-8859
                http://orcid.org/0000-0003-4212-3212
                http://orcid.org/0000-0001-6549-3713
                http://orcid.org/0000-0001-9258-2017
                http://orcid.org/0000-0002-0388-4177
                http://orcid.org/0000-0002-0081-6048
                http://orcid.org/0000-0001-6681-6844
                http://orcid.org/0000-0002-4838-3384
                http://orcid.org/0000-0001-5480-0888
                http://orcid.org/0000-0003-3413-5977
                http://orcid.org/0000-0002-1626-2465
                Article
                1995
                10.1038/s41398-022-01995-x
                9170720
                09492ff4-3ecc-4a0b-bdcb-a1ae7219e455
                © The Author(s) 2022

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 21 January 2022
                : 18 May 2022
                : 25 May 2022
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                © The Author(s) 2022

                Clinical Psychology & Psychiatry
                depression,diagnostic markers
                Clinical Psychology & Psychiatry
                depression, diagnostic markers

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