Frequency-resolved connectome alterations in major depressive disorder: A multisite resting fMRI study

Lei Wang; Qing Ma; Xiaoyi Sun; Zhilei Xu; Jiaying Zhang; Xuhong Liao; Xiaoqin Wang; Dongtao Wei; Yuan Chen; Bangshan Liu; Chu-Chung Huang; Yanting Zheng; Yankun Wu; Taolin Chen; Yuqi Cheng; Xiufeng Xu; Qiyong Gong; Tianmei Si; Shijun Qiu; Ching-Po Lin; Jingliang Cheng; Yanqing Tang; Fei Wang; Jiang Qiu; Peng Xie; Lingjiang Li; Yong He; DIDA-MDD Working Group; Mingrui Xia; Yihe Zhang

doi:10.1016/j.jad.2023.01.104

Frequency-resolved connectome alterations in major depressive disorder: A multisite resting fMRI study

J Affect Disord. 2023 May 1:328:47-57. doi: 10.1016/j.jad.2023.01.104. Epub 2023 Feb 11.

Authors

Lei Wang¹, Qing Ma², Xiaoyi Sun³, Zhilei Xu¹, Jiaying Zhang¹, Xuhong Liao⁴, Xiaoqin Wang⁵, Dongtao Wei⁵, Yuan Chen⁶, Bangshan Liu⁷, Chu-Chung Huang⁸, Yanting Zheng⁹, Yankun Wu¹⁰, Taolin Chen¹¹, Yuqi Cheng¹², Xiufeng Xu¹³, Qiyong Gong¹⁴, Tianmei Si¹⁰, Shijun Qiu⁹, Ching-Po Lin¹⁵, Jingliang Cheng⁶, Yanqing Tang¹⁶, Fei Wang¹⁶, Jiang Qiu⁵, Peng Xie¹⁷, Lingjiang Li⁷, Yong He¹⁸; DIDA-MDD Working Group; Mingrui Xia²⁷, Yihe Zhang²⁸

Collaborators

DIDA-MDD Working Group:
Yong He¹⁹, Lingjiang Li²⁰, Jingliang Cheng²¹, Qiyong Gong²², Lingjiang Li²⁰, Ching-Po Lin²³, Jiang Qiu²⁴, Shijun Qiu⁸, Tianmei Si⁹, Yanqing Tang²⁵, Fei Wang²⁵, Peng Xie²⁶, Xiufeng Xu¹¹, Mingrui Xia¹

Affiliations

¹ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China.
² Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Fudan University, Shanghai, China; MOE Frontiers Center for Brain Science, Fudan University, Shanghai, China.
³ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China; School of Systems Science, Beijing Normal University, Beijing, China.
⁴ School of Systems Science, Beijing Normal University, Beijing, China.
⁵ Key Laboratory of Cognition and Personality (SWU), Ministry of Education, Chongqing, China; Department of Psychology, Southwest University, Chongqing, China.
⁶ Department of Magnetic Resonance Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China.
⁷ Department of Psychiatry, National Clinical Research Center for Mental Disorders, The Second Xiangya Hospital of Central South University, Changsha, Hunan, China; Mental Health Institute of Central South University, China National Technology Institute on Mental Disorders, Hunan Key Laboratory of Psychiatry and Mental Health, Hunan Medical Center for Mental Health, Changsha, Hunan, China.
⁸ Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Cognitive Neuroscience, School of Psychology and Cognitive Science, East China Normal University, Shanghai, China.
⁹ Department of Radiology, The First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, China.
¹⁰ Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, China.
¹¹ Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital, Sichuan University, Chengdu, China.
¹² Department of Psychiatry, First Affiliated Hospital of Kunming Medical University, Kunming, China.
¹³ Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China.
¹⁴ Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital, Sichuan University, Chengdu, China; Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China.
¹⁵ Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London, UK; Institute of Neuroscience, National Yang-Ming Chiao-Tung University, Taipei, Taiwan.
¹⁶ Department of Psychiatry, The First Affiliated Hospital of China Medical University, Shenyang, China.
¹⁷ Chongqing Key Laboratory of Neurobiology, Chongqing, China; Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China.
¹⁸ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China; Chinese Institute for Brain Research, Beijing, China.
¹⁹ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China; Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China.
²⁰ Department of Magnetic Resonance Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China; Department of Psychiatry, National Clinical Research Center for Mental Disorders, The Second Xiangya Hospital of Central South University, Changsha, Hunan, China.
²¹ Department of Psychology, Southwest University, Chongqing, China.
²² Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, China; Department of Psychiatry, First Affiliated Hospital of Kunming Medical University, Kunming, China.
²³ Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China; Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London, UK.
²⁴ School of Systems Science, Beijing Normal University, Beijing, China; Key Laboratory of Cognition and Personality (SWU), Ministry of Education, Chongqing, China.
²⁵ Institute of Neuroscience, National Yang-Ming Chiao-Tung University, Taipei, Taiwan.
²⁶ Department of Psychiatry, The First Affiliated Hospital of China Medical University, Shenyang, China; Chongqing Key Laboratory of Neurobiology, Chongqing, China.
²⁷ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China. Electronic address: mxia@bnu.edu.cn.
²⁸ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China. Electronic address: amosyhzhang1989@gmail.com.

PMID: 36781144
DOI: 10.1016/j.jad.2023.01.104

Abstract

Background: Functional connectome studies have revealed widespread connectivity alterations in major depressive disorder (MDD). However, the low frequency bandpass filtering (0.01-0.08 Hz or 0.01-0.1 Hz) in most studies have impeded our understanding on whether and how these alterations are affected by frequency of interest.

Methods: Here, we performed frequency-resolved (0.01-0.06 Hz, 0.06-0.16 Hz and 0.16-0.24 Hz) connectome analyses using a large-sample resting-state functional MRI dataset of 1002 MDD patients and 924 healthy controls from seven independent centers.

Results: We reported significant frequency-dependent connectome alterations in MDD in left inferior parietal, inferior temporal, precentral, and fusiform cortices and bilateral precuneus. These frequency-dependent connectome alterations are mainly derived by abnormalities of medium- and long-distance connections and are brain network-dependent. Moreover, the connectome alteration of left precuneus in high frequency band (0.16-0.24 Hz) is significantly associated with illness duration.

Limitations: Multisite harmonization model only removed linear site effects. Neurobiological underpinning of alterations in higher frequency (0.16-0.24 Hz) should be further examined by combining fMRI data with respiration, heartbeat and blood flow recordings in future studies.

Conclusions: These results highlight the frequency-dependency of connectome alterations in MDD and the benefit of examining connectome alteration in MDD under a wider frequency band.

Keywords: Frequency; Functional connectivity strength; Major depressive disorder; Resting-state functional magnetic resonance imaging.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain
Cerebral Cortex
Connectome* / methods
Depressive Disorder, Major*
Humans
Magnetic Resonance Imaging / methods