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Gray matter atrophy is constrained by normal structural brain network architecture in depression

Published online by Cambridge University Press:  10 November 2023

Shaoqiang Han Open the ORCID record for Shaoqiang Han [Opens in a new window] ,
Keke Fang ,
Ruiping Zheng ,
Shuying Li ,
Bingqian Zhou ,
Wei Sheng ,
Baohong Wen ,
Liang Liu ,
Yarui Wei  and
Yuan Chen
...Show all authors
Shaoqiang Han
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Keke Fang
Affiliation:
Department of Pharmacy, Affiliated Cancer Hospital of Zhengzhou University, Henan Cancer Hospital, Zhengzhou, China
Ruiping Zheng
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Shuying Li
Affiliation:
Department of Psychiatry, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Bingqian Zhou
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Wei Sheng
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu, 610054, PR China
Baohong Wen
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Liang Liu
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Yarui Wei
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Yuan Chen*
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Huafu Chen*
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China The Clinical Hospital of Chengdu Brain Science Institute, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu, 610054, PR China
Qian Cui*
Affiliation:
School of Public Affairs and Administration, University of Electronic Science and Technology of China, Chengdu, China
Jingliang Cheng*
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
Yong Zhang*
Affiliation:
Department of Magnetic Resonance Imaging, the First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Key Laboratory for Functional Magnetic Resonance Imaging and Molecular Imaging of Henan Province, Zhengzhou, China Engineering Technology Research Center for Detection and Application of Brain Function of Henan Province, Zhengzhou, China Engineering Research Center of Medical Imaging Intelligent Diagnosis and Treatment of Henan Province, Zhengzhou, China Key Laboratory of Magnetic Resonance and Brain Function of Henan Province, Zhengzhou, China Key Laboratory of Brain Function and Cognitive Magnetic Resonance Imaging of Zhengzhou, Zhengzhou, China Key Laboratory of Imaging Intelligence Research Medicine of Henan Province, Zhengzhou, China Henan Engineering Research Center of Brain Function Development and Application, Zhengzhou, China
*
Corresponding authors: Yong Zhang; Email: zzuzhangyong2013@163.com; Jingliang Cheng; Email: fccchengjl@zzu.edu.cn; Qian Cui; Email: qiancui26@gmail.com; Huafu Chen; Email: chenhf@uestc.edu.cn; Yuan Chen; Email: chenyuanshizt@163.com
Corresponding authors: Yong Zhang; Email: zzuzhangyong2013@163.com; Jingliang Cheng; Email: fccchengjl@zzu.edu.cn; Qian Cui; Email: qiancui26@gmail.com; Huafu Chen; Email: chenhf@uestc.edu.cn; Yuan Chen; Email: chenyuanshizt@163.com
Corresponding authors: Yong Zhang; Email: zzuzhangyong2013@163.com; Jingliang Cheng; Email: fccchengjl@zzu.edu.cn; Qian Cui; Email: qiancui26@gmail.com; Huafu Chen; Email: chenhf@uestc.edu.cn; Yuan Chen; Email: chenyuanshizt@163.com
Corresponding authors: Yong Zhang; Email: zzuzhangyong2013@163.com; Jingliang Cheng; Email: fccchengjl@zzu.edu.cn; Qian Cui; Email: qiancui26@gmail.com; Huafu Chen; Email: chenhf@uestc.edu.cn; Yuan Chen; Email: chenyuanshizt@163.com
Corresponding authors: Yong Zhang; Email: zzuzhangyong2013@163.com; Jingliang Cheng; Email: fccchengjl@zzu.edu.cn; Qian Cui; Email: qiancui26@gmail.com; Huafu Chen; Email: chenhf@uestc.edu.cn; Yuan Chen; Email: chenyuanshizt@163.com
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Abstract

Background

There is growing evidence that gray matter atrophy is constrained by normal brain network (or connectome) architecture in neuropsychiatric disorders. However, whether this finding holds true in individuals with depression remains unknown. In this study, we aimed to investigate the association between gray matter atrophy and normal connectome architecture at individual level in depression.

Methods

In this study, 297 patients with depression and 256 healthy controls (HCs) from two independent Chinese dataset were included: a discovery dataset (105 never-treated first-episode patients and matched 130 HCs) and a replication dataset (106 patients and matched 126 HCs). For each patient, individualized regional atrophy was assessed using normative model and brain regions whose structural connectome profiles in HCs most resembled the atrophy patterns were identified as putative epicenters using a backfoward stepwise regression analysis.

Results

In general, the structural connectome architecture of the identified disease epicenters significantly explained 44% (±16%) variance of gray matter atrophy. While patients with depression demonstrated tremendous interindividual variations in the number and distribution of disease epicenters, several disease epicenters with higher participation coefficient than randomly selected regions, including the hippocampus, thalamus, and medial frontal gyrus were significantly shared by depression. Other brain regions with strong structural connections to the disease epicenters exhibited greater vulnerability. In addition, the association between connectome and gray matter atrophy uncovered two distinct subgroups with different ages of onset.

Conclusions

These results suggest that gray matter atrophy is constrained by structural brain connectome and elucidate the possible pathological progression in depression.

Keywords

depressionheterogeneitysubtypes of depressionindividualized analysisgray matter volumemulti-modalmulti-center datasetsepicenternormative modelfunctional connectivitystructural covariance networksubtypes
Type
Original Article
Information
Psychological Medicine , Volume 54 , Issue 7 , May 2024 , pp. 1318 - 1328
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Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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Footnotes

*

Shaoqiang Han and Keke Fang contributed to the work equally and should be regarded as co- pioneer first authors.

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