Population clustering of structural brain aging and its association with brain development.

Humans Brain / growth & development Aging / physiology Female Male Longitudinal Studies Adolescent Middle Aged Cross-Sectional Studies Aged Neuroimaging United Kingdom Magnetic Resonance Imaging Adult Cluster Analysis
MRI adolescence genetics genomics human longitudinal analysis neuroscience structural brain aging

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
18 Oct 2024
Historique:
medline: 18 10 2024
pubmed: 18 10 2024
entrez: 18 10 2024
Statut: epublish

Résumé

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.

Identifiants

DOI: 10.7554/eLife.94970 PMID: 39422662
pubmed: 39422662
doi: 10.7554/eLife.94970
pii: 94970
doi:
pii:

Banques de données

Dryad
['10.5061/dryad.jh9w0vtmn']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : No.82304241
Organisme : National Key Research and Development Program of China
ID : No.2019YFA0709502
Organisme : National Key Research and Development Program of China
ID : No.2018YFC1312904
Organisme : Shanghai Municipal Science and Technology Major Project
ID : No.2018SHZDZX01
Organisme : 111 project
ID : No.B18015
Organisme : European Union FP6 Integrated Project IMAGEN
ID : LSHM-CT- 2007-037286
Organisme : Horizon 2020 ERC Advanced Grant 'STRATIFY'
ID : 695313
Organisme : Human Brain Project
ID : HBP SGA 2,785907
Organisme : Human Brain Project
ID : HBP SGA 3,945539
Organisme : Medical Research Council Grant 'c-VEDA'
ID : MR/N000390/1
Organisme : NIH HHS
ID : R01DA049238
Pays : United States
Organisme : Deutsche Forschungsgemeinschaft
ID : SM 80/7-2
Organisme : Medical Research Foundation and Medical Research Council
ID : MR/R00465X/1
Organisme : NIH HHS
ID : ENIGMA 5U54EB020403-05
Pays : United States
Organisme : NIH HHS
ID : U54 EB020403
Pays : United States
Organisme : ANR
ID : ANR-12-SAMA-0004 AAPG2019 - GeBra
Organisme : Eranet Neuron
ID : AF12-NEUR0008-01 - WM2NA
Organisme : Fondation de France
ID : 00081242
Organisme : Fondation pour la Recherche Médicale
ID : DPA20140629802
Organisme : Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives
ID : MILDECA
Organisme : Assistance-Publique-Hôpitaux-de-Paris and INSERM
ID : interface grant
Organisme : Fondation de l'Avenir
ID : AP-RM-17-013
Organisme : National Institutes of Health, Science Foundation Ireland
ID : 16/ERCD/3797
Organisme : NSFC
ID : 82150710554
Organisme : environMENTAL
ID : grant no: 101057429
Organisme : Bundesministeriumfür Bildung und Forschung
ID : 01GS08152
Organisme : Bundesministeriumfür Bildung und Forschung
ID : 01EV0711
Organisme : Forschungsnetz AERIAL
ID : 01EE1406A
Organisme : Forschungsnetz AERIAL
ID : 01EE1406B
Organisme : Forschungsnetz IMAC-Mind
ID : 01GL1745B
Organisme : Deutsche Forschungsgemeinschaft
ID : SFB 940
Organisme : Deutsche Forschungsgemeinschaft
ID : TRR 265
Organisme : Deutsche Forschungsgemeinschaft
ID : NE 1383/14-1
Organisme : Medical Research Foundation and Medical Research Council
ID : MR/S020306/1
Organisme : NIH HHS
ID : ENIGMA 1R56AG058854-01
Pays : United States
Organisme : Eranet
ID : ANR-18-NEUR00002-01 - ADORe

Informations de copyright

© 2024, Duan et al.

Déclaration de conflit d'intérêts

HD, RS, JK, AB, SD, HF, AG, HG, PG, AH, RB, JM, MM, EA, FN, DP, SH, NN, JF, MS, NV, HW, RW, GS, XL, JF No competing interests declared, TB Dr Banaschewski served in an advisory or consultancy role for eye level, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker's fee by Janssen, Medice and Takeda. He received royalities from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press; the presentwork is unrelated to these relationships, CB Reviewing editor, eLife, LP Dr Poustka served in an advisory or consultancy role for Roche and Viforpharm and received speaker's fee by Shire. She received royalties from Hogrefe, Kohlhammer and Schattauer. The present work is unrelated to the above grants and relationships

Auteurs

Haojing Duan (H)

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.
ORCID: 0009-0004-8659-9591

Runye Shi (R)

School of Data Science, Fudan University, Shanghai, China.

Jujiao Kang (J)

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 (T)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Arun L W Bokde (ALW)

Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.

Christian Büchel (C)

University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
ORCID: 0000-0003-1965-906X

Sylvane Desrivières (S)

Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.

Herta Flor (H)

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 (A)

NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France.

Hugh Garavan (H)

Departments of Psychiatry and Psychology, University of Vermont, Burlington, United States.

Penny A Gowland (PA)

Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom.

Andreas Heinz (A)

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 (R)

Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Berlin, Germany.
ORCID: 0000-0003-0111-5996

Jean-Luc Martinot (JL)

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.
ORCID: 0000-0002-0136-0388

Marie-Laure Paillère Martinot (MP)

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 (E)

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 (F)

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 (D)

NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France.
ORCID: 0000-0002-1242-8990

Luise Poustka (L)

Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre, Göttingen, Germany.

Sarah Hohmann (S)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Nathalie Nathalie Holz (N)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Juliane Fröhner (J)

Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.

Michael N Smolka (MN)

Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
ORCID: 0000-0001-5398-5569

Nilakshi Vaidya (N)

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 (H)

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 (R)

School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.

Gunter Schumann (G)

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 (X)

School of Data Science, Fudan University, Shanghai, China.
Huashan Institute of Medicine, Huashan Hospital affiliated to Fudan University, Shanghai, China.
ORCID: 0000-0003-2463-1272

Jianfeng Feng (J)

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.
ORCID: 0000-0001-5987-2258

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