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Age- and gender-related dispersion of brain networks across the lifespan

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Abstract

The effects of age and gender on large-scale resting-state networks (RSNs) reflecting within- and between-network connectivity in the healthy brain remain unclear. This study investigated how age and gender influence the brain network roles and topological properties underlying the ageing process. Ten RSNs were constructed based on 998 participants from the REST-meta-MDD cohort. Multivariate linear regression analysis was used to examine the independent and interactive influences of age and gender on large-scale RSNs and their topological properties. A support vector regression model integrating whole-brain network features was used to predict brain age across the lifespan and cognitive decline in an Alzheimer’s disease spectrum (ADS) sample. Differential effects of age and gender on brain network roles were demonstrated across the lifespan. Specifically, cingulo-opercular, auditory, and visual (VIS) networks showed more incohesive features reflected by decreased intra-network connectivity with ageing. Further, females displayed distinctive brain network trajectory patterns in middle-early age, showing enhanced network connectivity within the fronto-parietal network (FPN) and salience network (SAN) and weakened network connectivity between the FPN-somatomotor, FPN-VIS, and SAN-VIS networks. Age — but not gender — induced widespread decrease in topological properties of brain networks. Importantly, these differential network features predicted brain age and cognitive impairment in the ADS sample. By showing that age and gender exert specific dispersion of dynamic network roles and trajectories across the lifespan, this study has expanded our understanding of age- and gender-related brain changes with ageing. Moreover, the findings may be useful for detecting early-stage dementia.

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Acknowledgements

We thank the Depression Imaging REsearch ConsorTium for sharing data. We would like to thank MogoEdit (https://www.mogoedit.com) for its English editing during the preparation of this manuscript.

Consortium name: Depression Imaging REsearch ConsorTium

Chao-Gan Yan (Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China; Magnetic Resonance Imaging Research Center and Research Center for Lifespan Development of Mind and Brain, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, US), Xiao Chen (Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China), Le Li (Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China), Francisco Xavier Castellanos (Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, US; Nathan Kline Institute for Psychiatric Research, Orangeburg, US), Tong-Jian Bai (Anhui Medical University, Anhui, China), Qi-Jing Bo (Beijing Anding Hospital, Capital Medical University, Beijing, China), Guan-Mao Chen (The First Affiliated Hospital of Jinan University, Guangzhou, Guangdong, China), Ning-Xuan Chen (Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China), Wei Chen (Department of Psychiatry, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China), Chang Cheng (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Yu-Qi Cheng (First Affiliated Hospital of Kunming Medical University, Kunming, Yunnan, China), Xi-Long Cui (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Jia Duan (Department of Psychiatry, First Affiliated Hospital, China Medical University, Liaoning, China), Yi-Ru Fang (Department of Psychiatry, Shanghai Jiao Tong University School of Medicine, Shanghai, China), Qi-Yong Gong (Department of Radiology, Huaxi MR Research Center, West China Hospital of Sichuan University, Sichuan, China; Psychoradiology Research Unit of Chinese Academy of Medical Sciences, West China Hospital of Sichuan University, Sichuan, China), Wen-Bin Guo (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Zheng-Hua Hou (Department of Psychosomatics and Psychiatry, Zhongda Hospital, School of Medicine, Southeast University, Jiangsu, China), Lan Hu (Department of Psychiatry, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China), Li Kuang (Department of Psychiatry, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China), Feng Li (Beijing Anding Hospital, Capital Medical University, Beijing 100,054, China), Kai-Ming Li (Department of Radiology, Huaxi MR Research Center, West China Hospital of Sichuan University, Sichuan, China), Tao Li (Mental Health Center, West China Hospital, Sichuan University, Sichuan, China), Yan-Song Liu (Department of Clinical Psychology, Suzhou Psychiatric Hospital, The Affiliated Guangji Hospital of Soochow University, Jiangsu, China), Zhe-Ning Liu (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Yi-Cheng Long (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Qing-Hua Luo (Department of Psychiatry, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China), Hua-Qing Meng (Department of Psychiatry, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China), Dai-Hui Peng (Department of Psychiatry, Shanghai Jiao Tong University School of Medicine, Shanghai, China), Hai-Tang Qiu (Department of Psychiatry, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China), Jiang Qiu (Faculty of Psychology, Southwest University, Chongqing, China), Yue-Di Shen (Department of Radiology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Zhejiang, China), Yu-Shu Shi (Xi’an Central Hospital, Shaanxi, China), Chuan-Yue Wang (Beijing Anding Hospital, Capital Medical University, Beijing, China), Fei Wang (Department of Psychiatry, First Affiliated Hospital, China Medical University, Liaoning, China), Kai Wang (Anhui Medical University, Anhui, China), Li Wang (National Clinical Research Center for Mental Disorders, Peking University Sixth Hospital, Beijing, China; Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China), Xiang Wang (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Ying Wang (The First Affiliated Hospital of Jinan University, Guangdong, China), Xiao-Ping Wu (Xi’an Central Hospital, Shaanxi, China), Xin-Ran Wu (Faculty of Psychology, Southwest University, Chongqing, China), Guang-Rong Xie (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Hai-Yan Xie (Department of Psychiatry, The Fourth Affiliated Hospital, College of Medicine, Zhejiang University, Zhejiang, China), Peng Xie (Institute of Neuroscience, Chongqing Medical University, Chongqing, China; Chongqing Key Laboratory of Neurobiology, Chongqing, China; and Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China), Xiu-Feng Xu (First Affiliated Hospital of Kunming Medical University, Yunnan, China), Hong Yang (Department of Radiology, the First Affiliated Hospital, College of Medicine, Zhejiang University, Zhejiang, China), Jian Yang (The First Affiliated Hospital of Xi’an Jiaotong University, Shanxi, China), Jia-Shu Yao (Department of Psychiatry, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Zhejiang, China), Shu-Qiao Yao (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Ying-Ying Yin (Department of Psychosomatics and Psychiatry, Zhongda Hospital, School of Medicine, Southeast University, Jiangsu, China), Yong-Gui Yuan (Department of Psychosomatics and Psychiatry, Zhongda Hospital, School of Medicine, Southeast University, Jiangsu, China), Ai-Xia Zhang (The First Affiliated Hospital of Xi’an Jiaotong University, Shanxi, China), Hong Zhang (Xi’an Central Hospital, Shaanxi, China), Ke-Rang Zhang (First Hospital of Shanxi Medical University, Shanxi, China), Lei Zhang (Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China), Ru-Bai Zhou (Department of Psychiatry, Shanghai Jiao Tong University School of Medicine, Shanghai, China), Yi-Ting Zhou (Mental Health Center, West China Hospital, Sichuan University, Sichuan, China), Jun-Juan Zhu (Department of Psychiatry, Shanghai Jiao Tong University School of Medicine, Shanghai, China), Chao-Jie Zou (First Affiliated Hospital of Kunming Medical University, Yunnan, China), Tian-Mei Si (National Clinical Research Center for Mental Disorders, Peking University Sixth Hospital, Beijing, China; and Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China), Xi-Nian Zuo (Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China; and Magnetic Resonance Imaging Research Center and Research Center for Lifespan Development of Mind and Brain, Institute of Psychology, Chinese Academy of Sciences, Beijing, China), Jing-Ping Zhao (Department of Psychiatry, The Second Xiangya Hospital of Central South University, Wuhan, China), Yu-Feng Zang (Center for Cognition and Brain Disorders, Institutes of Psychological Sciences, Hangzhou Normal University, Zhejiang, China; and Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, Zhejiang, China) and Chunming Xie (Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Southeast University, Jiangsu, China; Institute of Neuropsychiatry, Affiliated ZhongDa Hospital, Southeast University, Jiangsu, China; and the Key Laboratory of Developmental Genes and Human Disease, Southeast University, Jiangsu, China).

Funding

This research was funded by the Science and Technology Innovation 2030 Major Projects (2022ZD0211600, CMX), the National Natural Science Foundation of China (82271574, 82071204, 81871069, CMX), the Foundation of Jiangsu Commission of Health (Z2018023, CMX), and Jiangsu Province Health Management Department of China (H2020080, HXF).

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Author notes

  1. Cancan He

    Present address: Institute of Neuropsychiatry, Affiliated ZhongDa Hospital, Southeast University, Nanjing, Jiangsu, 210009, China

  2. Qing Wang and Lingyu Qi contributed equally to this manuscript.

Authors and Affiliations

  1. Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Southeast University, Nanjing, Jiangsu, 210009, China

    Qing Wang, Lingyu Qi, Cancan He & Chunming Xie

  2. Institute of Neuropsychiatry, Affiliated ZhongDa Hospital, Southeast University, Nanjing, Jiangsu, 210009, China

    Chunming Xie

  3. Department of Nursing, Affiliated ZhongDa Hospital, School of Medicine, Southeast University, Nanjing, Jiangsu, 210009, China

    Haixia Feng

  4. The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu, 210096, China

    Chunming Xie

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  1. Qing Wang
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Consortia

Depression Imaging REsearch ConsorTium

  • Chao-Gan Yan
  • , Xiao Chen
  • , Le Li
  • , Francisco Xavier Castellanos
  • , Tong-Jian Bai
  • , Ning-Xuan Chen
  • , Wei Chen
  • , Chang Cheng
  • , Yu-Qi Cheng
  • , Xi-Long Cui
  • , Jia Duan
  • , Yi-Ru Fang
  • , Qi-Yong Gong
  • , Wen-Bin Guo
  • , Zheng-Hua Hou
  • , Lan Hu
  • , Li Kuang
  • , Feng Li
  • , Kai-Ming Li
  • , Tao Li
  • , Yan-Song Liu
  • , Zhe-Ning Liu
  • , Yi-Cheng Long
  • , Qing-Hua Luo
  • , Hua-Qing Meng
  • , Dai-Hui Peng
  • , Hai-Tang Qiu
  • , Jiang Qiu
  • , Yue-Di Shen
  • , Yu-Shu Shi
  • , Chuan-Yue Wang
  • , Fei Wang
  • , Kai Wang
  • , Li Wang
  • , Xiang Wang
  • , Ying Wang
  • , Xiao-Ping Wu
  • , Xin-Ran Wu
  • , Guang-Rong Xie
  • , Hai-Yan Xie
  • , Peng Xie
  • , Xiu-Feng Xu
  • , Hong Yang
  • , Jian Yang
  • , Jia-Shu Yao
  • , Shu-Qiao Yao
  • , Ying-Ying Yin
  • , Yong-Gui Yuan
  • , Ai-Xia Zhang
  • , Hong Zhang
  • , Ke-Rang Zhang
  • , Lei Zhang
  • , Ru-Bai Zhou
  • , Yi-Ting Zhou
  • , Jun-Juan Zhu
  • , Chao-Jie Zou
  • , Tian-Mei Si
  • , Xi-Nian Zuo
  • , Jing-Ping Zhao
  • , Yu-Feng Zang
  •  & Chunming Xie

Contributions

All authors have made substantial intellectual contributions to this manuscript. Dr. Xie took the conceptualization, analysis, and revision of this manuscript. Ms. Qi, Ms. He and Ms. Feng conducted the data collection and preparation. Ms. Wang and Ms. Qi conducted the analysis, investigation, visualization, and writing of this manuscript. All authors have given final approval of this manuscript.

Corresponding author

Correspondence to Chunming Xie.

Ethics declarations

Competing interests

The authors declare no competing interests. The funders had no role in the design of the study, or in the collection, analyses, or interpretation of data, or in the writing of the manuscript, or in the decision to publish the results.

Additional information

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The data used in preparing this article were parted from the Depression Imaging REsearch ConsorTium.

Supplementary Information

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Cite this article

Wang, Q., Qi, L., He, C. et al. Age- and gender-related dispersion of brain networks across the lifespan. GeroScience 46, 1303–1318 (2024). https://doi.org/10.1007/s11357-023-00900-8

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  • DOI: https://doi.org/10.1007/s11357-023-00900-8

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