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Regional patterns of human cortex development correlate with underlying neurobiology

Affiliations
  • 1Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany. l.lotter@fz-juelich.de.
  • 2Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany. l.lotter@fz-juelich.de.
  • 3Max Planck School of Cognition; Stephanstrasse 1A, Leipzig, Germany. l.lotter@fz-juelich.de.
  • 4Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany.
  • 5Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany.
  • 6Otto Hahn Research Group for Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
  • 7McConnell Brain Imaging Centre, Montréal Neurological Institute, McGill University, Montréal, QC, Canada.
  • 8Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK.
  • 9Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
  • 10Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, UK.
  • 11Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
  • 12Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany.
  • 13NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France.
  • 14Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, USA.
  • 15Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham; University Park, Nottingham, UK.
  • 16Department 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.
  • 17Physikalisch-Technische Bundesanstalt (PTB); Braunschweig and Berlin, Berlin, Germany.
  • 18AP-HP Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
  • 19Department of Psychiatry, EPS Barthélémy Durand, Etampes, France.
  • 20Departments of Psychiatry and Neuroscience, Faculty of Medicine and Centre Hospitalier Universitaire Sainte-Justine, University of Montreal, Montréal, QC, Canada.
  • 21Department of Psychiatry, McGill University, Montreal, QC, Canada.
  • 22Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, Göttingen, Germany.
  • 23Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
  • 24Department of Psychiatry and Psychotherapy, Technische Universität Dresden, Dresden, Germany.
  • 25Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin Berlin, Berlin, Germany.
  • 26School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
  • 27Centre for Population Neuroscience and Precision Medicine (PONS), Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China.
  • 28Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany.
  • 29German Center for Mental Health (DZPG), partner site Mannheim-Heidelberg-Ulm, Heidelberg, Germany.
  • 30Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany. juergen.dukart@gmail.com.
  • 31Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany. juergen.dukart@gmail.com.

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September 16, 2024

Abstract

Human brain morphology undergoes complex changes over the lifespan. Despite recent progress in tracking brain development via normative models, current knowledge of underlying biological mechanisms is highly limited. We demonstrate that human cortical thickness development and aging trajectories unfold along patterns of molecular and cellular brain organization, traceable from population-level to individual developmental trajectories. During childhood and adolescence, cortex-wide spatial distributions of dopaminergic receptors, inhibitory neurons, glial cell populations, and brain-metabolic features explain up to 50% of the variance associated with a lifespan model of regional cortical thickness trajectories. In contrast, modeled cortical thickness change patterns during adulthood are best explained by cholinergic and glutamatergic neurotransmitter receptor and transporter distributions. These relationships are supported by developmental gene expression trajectories and translate to individual longitudinal data from over 8000 adolescents, explaining up to 59% of developmental change at cohort- and 18% at single-subject level. Integrating neurobiological brain atlases with normative modeling and population neuroimaging provides a biologically meaningful path to understand brain development and aging in living humans.

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