eLife (Oct 2024)
Population clustering of structural brain aging and its association with brain development
- Haojing Duan,
- Runye Shi,
- Jujiao Kang,
- Tobias Banaschewski,
- Arun LW Bokde,
- Christian Büchel,
- Sylvane Desrivières,
- Herta Flor,
- Antoine Grigis,
- Hugh Garavan,
- Penny A Gowland,
- Andreas Heinz,
- Rüdiger Brühl,
- Jean-Luc Martinot,
- Marie-Laure Paillère Martinot,
- Eric Artiges,
- Frauke Nees,
- Dimitri Papadopoulos Orfanos,
- Luise Poustka,
- Sarah Hohmann,
- Nathalie Nathalie Holz,
- Juliane Fröhner,
- Michael N Smolka,
- Nilakshi Vaidya,
- Henrik Walter,
- Robert Whelan,
- Gunter Schumann,
- Xiaolei Lin,
- Jianfeng Feng
Affiliations
- Haojing Duan
- ORCiD
- Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China
- Runye Shi
- School of Data Science, Fudan University, Shanghai, China
- Jujiao Kang
- Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China
- Tobias Banaschewski
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
- Arun LW Bokde
- Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland
- Christian Büchel
- ORCiD
- University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
- Sylvane Desrivières
- Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
- Herta Flor
- Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany
- Antoine Grigis
- NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France
- Hugh Garavan
- Departments of Psychiatry and Psychology, University of Vermont, Burlington, United States
- Penny A Gowland
- Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom
- Andreas Heinz
- Department of Psychiatry and Psychotherapy CCM, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Rüdiger Brühl
- ORCiD
- Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Berlin, Germany
- Jean-Luc Martinot
- ORCiD
- Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental Trajectories and Psychiatry", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France
- Marie-Laure Paillère Martinot
- Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental Trajectories and Psychiatry", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France; AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France
- Eric Artiges
- Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental Trajectories and Psychiatry", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France; Psychiatry Department, EPS Barthélémy Durand, Etampes, France
- Frauke Nees
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany
- Dimitri Papadopoulos Orfanos
- ORCiD
- NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France
- Luise Poustka
- Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre, Göttingen, Germany
- Sarah Hohmann
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
- Nathalie Nathalie Holz
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
- Juliane Fröhner
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
- Michael N Smolka
- ORCiD
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
- Nilakshi Vaidya
- Department of Psychiatry and Neurosciences, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität BerlinHumboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Henrik Walter
- Department of Psychiatry and Psychotherapy CCM, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Robert Whelan
- School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland
- Gunter Schumann
- Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Department of Psychiatry and Neurosciences, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität BerlinHumboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Centre for Population Neuroscience and Stratified Medicine (PONS Centre), ISTBI, Fudan University, Shanghai, China; Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Psychotherapy, Charité Universitätsmedizin, Berlin, Germany
- Xiaolei Lin
- ORCiD
- School of Data Science, Fudan University, Shanghai, China; Huashan Institute of Medicine, Huashan Hospital affiliated to Fudan University, Shanghai, China
- Jianfeng Feng
- ORCiD
- Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China; School of Data Science, Fudan University, Shanghai, China; Centre for Population Neuroscience and Stratified Medicine (PONS Centre), ISTBI, Fudan University, Shanghai, China; MOE Frontiers Center for Brain Science, Fudan University, Shanghai, China; Zhangjiang Fudan International Innovation Center, Shanghai, China; Department of Computer Science, University of Warwick, Warwick, United Kingdom
- DOI
- https://doi.org/10.7554/eLife.94970
- Journal volume & issue
-
Vol. 13
Abstract
Structural brain aging has demonstrated strong inter-individual heterogeneity and mirroring patterns with brain development. However, due to the lack of large-scale longitudinal neuroimaging studies, most of the existing research focused on the cross-sectional changes of brain aging. In this investigation, we present a data-driven approach that incorporate both cross-sectional changes and longitudinal trajectories of structural brain aging and identified two brain aging patterns among 37,013 healthy participants from UK Biobank. Participants with accelerated brain aging also demonstrated accelerated biological aging, cognitive decline and increased genetic susceptibilities to major neuropsychiatric disorders. Further, by integrating longitudinal neuroimaging studies from a multi-center adolescent cohort, we validated the ‘last in, first out’ mirroring hypothesis and identified brain regions with manifested mirroring patterns between brain aging and brain development. Genomic analyses revealed risk loci and genes contributing to accelerated brain aging and delayed brain development, providing molecular basis for elucidating the biological mechanisms underlying brain aging and related disorders.
Keywords
