Hemispheric asymmetry in cortical thinning reflects intrinsic organization of the neurotransmitter systems and homotopic functional connectivity.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
17 10 2023
Historique:
pmc-release: 13 04 2024
medline: 1 11 2023
pubmed: 13 10 2023
entrez: 13 10 2023
Statut: ppublish

Résumé

Hemispheric lateralization and its origins have been of great interest in neuroscience for over a century. The left-right asymmetry in cortical thickness may stem from differential maturation of the cerebral cortex in the two hemispheres. Here, we investigated the spatial pattern of hemispheric differences in cortical thinning during adolescence, and its relationship with the density of neurotransmitter receptors and homotopic functional connectivity. Using longitudinal data from IMAGEN study (N = 532), we found that many cortical regions in the frontal and temporal lobes thinned more in the right hemisphere than in the left. Conversely, several regions in the occipital and parietal lobes thinned less in the right (vs. left) hemisphere. We then revealed that regions thinning more in the right (vs. left) hemispheres had higher density of neurotransmitter receptors and transporters in the right (vs. left) side. Moreover, the hemispheric differences in cortical thinning were predicted by homotopic functional connectivity. Specifically, regions with stronger homotopic functional connectivity showed a more symmetrical rate of cortical thinning between the left and right hemispheres, compared with regions with weaker homotopic functional connectivity. Based on these findings, we suggest that the typical patterns of hemispheric differences in cortical thinning may reflect the intrinsic organization of the neurotransmitter systems and related patterns of homotopic functional connectivity.

Identifiants

pubmed: 37831741
doi: 10.1073/pnas.2306990120
pmc: PMC10589642
doi:

Substances chimiques

Receptors, Neurotransmitter 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2306990120

Subventions

Organisme : MRF
ID : MRF_MRF-058-0004-RG-DESRI
Pays : United Kingdom
Organisme : NIH HHS
ID : R01MH085772
Pays : United States
Organisme : Department of Health
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : R01 MH085772
Pays : United States
Organisme : NIA NIH HHS
ID : R56 AG058854
Pays : United States
Organisme : Medical Research Council
ID : MR/W002418/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : MRF
ID : MRF_MRF-058-0009-RG-DESR-C0759
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N000390/1
Pays : United Kingdom
Organisme : NIDA NIH HHS
ID : R01 DA049238
Pays : United States
Organisme : Wellcome Trust
ID : 076467/Z/05/Z
Pays : United Kingdom
Organisme : NIBIB NIH HHS
ID : U54 EB020403
Pays : United States
Organisme : Medical Research Council
ID : MR/R00465X/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S020306/1
Pays : United Kingdom

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Auteurs

Zhijie Liao (Z)

Research Centre of Sainte-Justine University Hospital, Montreal, QC H3T 1C5, Canada.
Department of Psychiatry and Addictology, University of Montreal, Montreal, QC H3T 1J4, Canada.

Tobias Banaschewski (T)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 68159, Germany.

Arun L W Bokde (ALW)

Discipline of Psychiatry, School of Medicine, Trinity College Dublin, Dublin D02 PN40, Ireland.
Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin D02 PN40, Ireland.

Sylvane Desrivières (S)

Centre for Population Neuroscience and Precision Medicine, Institute of Psychiatry, Psychology & Neuroscience, Social, Genetic & Developmental Psychiatry Centre, King's College London, London SE5 8AF, United Kingdom.

Herta Flor (H)

Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 69117, Germany.
Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim 68131, Germany.

Antoine Grigis (A)

NeuroSpin, Energies and Atomic Energy Commission, Université Paris-Saclay, Paris F-91191, France.

Hugh Garavan (H)

Department of Psychiatry, University of Vermont, Burlington, VT 05405.
Department of Psychology, University of Vermont, Burlington, VT 05405.

Penny Gowland (P)

Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham NG7 2RD, United Kingdom.

Andreas Heinz (A)

Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin 10117, Germany.

Bernd Ittermann (B)

Physikalisch-Technische Bundesanstalt, Braunschweig and Berlin 38116, Germany.

Jean-Luc Martinot (JL)

Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental trajectories & psychiatry" Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Paris 75006, France.

Marie-Laure Paillère Martinot (ML)

Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental trajectories & psychiatry" Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Paris 75006, France.
Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, AP-HP.Sorbonne Université, Paris 75006, France.

Eric Artiges (E)

Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental trajectories & psychiatry" Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Paris 75006, France.
Etablissement Public de Santé Barthélemy Durand, Paris 91700, France.

Frauke Nees (F)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 68159, Germany.
Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 69117, Germany.
Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel 24118, Germany.

Dimitri Papadopoulos Orfanos (D)

NeuroSpin, Energies and Atomic Energy Commission, Université Paris-Saclay, Paris F-91191, France.

Luise Poustka (L)

Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, Göttingen 37075, Germany.

Sarah Hohmann (S)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 68159, Germany.

Sabina Millenet (S)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 68159, Germany.

Juliane H Fröhner (JH)

Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden 01087, Germany.

Michael N Smolka (MN)

Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden 01087, Germany.

Henrik Walter (H)

Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin 10117, Germany.

Robert Whelan (R)

School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin D02 PN40, Ireland.

Gunter Schumann (G)

Centre for Population Neuroscience and Precision Medicine, Institute of Psychiatry, Psychology & Neuroscience, Institute for Science and Technology of Brain-inspired Intelligence, Fudan University, Shanghai 200437, Peoples Republic of China.
Centre for Population Neuroscience and Precision Medicine, Charite Universitätsmedizin Berlin, Berlin 10117, Germany.

Tomáš Paus (T)

Research Centre of Sainte-Justine University Hospital, Montreal, QC H3T 1C5, Canada.
Department of Psychiatry and Addictology, University of Montreal, Montreal, QC H3T 1J4, Canada.
Department of Neuroscience, University of Montreal, Montreal, QC H3T 1J4, Canada.

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