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

Author:

Liao Zhijie12ORCID,Banaschewski Tobias3ORCID,Bokde Arun L. W.45,Desrivières Sylvane6ORCID,Flor Herta78ORCID,Grigis Antoine9,Garavan Hugh1011,Gowland Penny12ORCID,Heinz Andreas13ORCID,Ittermann Bernd14ORCID,Martinot Jean-Luc15ORCID,Paillère Martinot Marie-Laure1516ORCID,Artiges Eric1517ORCID,Nees Frauke3718ORCID,Papadopoulos Orfanos Dimitri9ORCID,Poustka Luise19ORCID,Hohmann Sarah3,Millenet Sabina3ORCID,Fröhner Juliane H.20ORCID,Smolka Michael N.20ORCID,Walter Henrik13ORCID,Whelan Robert21ORCID,Schumann Gunter2223,Paus Tomáš1224,Banaschewski Tobias,Barker Gareth J.,Bokde Arun L. W.,Flor Herta,Grigis Antoine,Garavan Hugh,Gowland Penny,Heinz Andreas,Brühl Rüdiger,Martinot Jean-Luc,Artiges Eric,Nees Frauke,Papadopoulos Orfanos Dimitri,Lemaitre Herve,Paus Tomáš,Poustka Luise,Robinson Lauren,Hohmann Sarah,Fröhner Juliane H.,Smolka Michael N.,Walter Henrik,Whelan Robert,Winterer Jeanne,Barker Edward D.,Schumann Gunter,

Affiliation:

1. Research Centre of Sainte-Justine University Hospital, Montreal, QC H3T 1C5, Canada

2. Department of Psychiatry and Addictology, University of Montreal, Montreal, QC H3T 1J4, Canada

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

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

5. Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin D02 PN40, Ireland

6. 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

7. Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim 69117, Germany

8. Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim 68131, Germany

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

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

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

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

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

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

15. 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

16. Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, AP-HP.Sorbonne Université, Paris 75006, France

17. Etablissement Public de Santé Barthélemy Durand, Paris 91700, France

18. Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel 24118, Germany

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

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

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

22. 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

23. Centre for Population Neuroscience and Precision Medicine, Charite Universitätsmedizin Berlin, Berlin 10117, Germany

24. Department of Neuroscience, University of Montreal, Montreal, QC H3T 1J4, Canada

Abstract

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.

Funder

Wellcome Trust and MRC

National Institutes of Health

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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