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Orbitofrontal cortex volume links polygenic risk for smoking with tobacco use in healthy adolescents

Published online by Cambridge University Press:  03 September 2020

Jin Li Open the ORCID record for Jin Li [Opens in a new window] ,
Bing Liu ,
Tobias Banaschewski ,
Arun L.W. Bokde ,
Erin Burke Quinlan ,
Sylvane Desrivières ,
Herta Flor ,
Vincent Frouin ,
Hugh Garavan  and
Penny Gowland
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Jin Li
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China
Bing Liu
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China University of Chinese Academy of Sciences, 19 Yuquan Road, Beijing, 100049, China
Tobias Banaschewski
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany
Arun L.W. Bokde
Affiliation:
Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland
Erin Burke Quinlan
Affiliation:
Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King's College London, London, UK
Sylvane Desrivières
Affiliation:
Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King's College London, London, UK
Herta Flor
Affiliation:
Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany Department of Psychology, School of Social Sciences, University of Mannheim, 68131 Mannheim, Germany
Vincent Frouin
Affiliation:
NeuroSpin, CEA, Université Paris-Saclay, F-91191 Gif-sur-Yvette, France
Hugh Garavan
Affiliation:
Departments of Psychiatry and Psychology, University of Vermont, 05405 Burlington, Vermont, USA
Penny Gowland
Affiliation:
Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, UK
Andreas Heinz
Affiliation:
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
Bernd Ittermann
Affiliation:
Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Germany
Jean-Luc Martinot
Affiliation:
Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 ‘Neuroimaging & Psychiatry’, University Paris-Saclay, University Paris Descartes – Sorbonne Paris Cité; and Maison de Solenn, Paris, France
Eric Artiges
Affiliation:
Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 ‘Neuroimaging & Psychiatry’, University Paris-Saclay, University Paris Descartes – Sorbonne Paris Cité; and Psychiatry Department 91G16, Orsay Hospital, Orsay, France
Frauke Nees
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany
Dimitri Papadopoulos Orfanos
Affiliation:
NeuroSpin, CEA, Université Paris-Saclay, F-91191 Gif-sur-Yvette, France
Tomáš Paus
Affiliation:
Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, Ontario, Canada Departments of Psychology and Psychiatry, University of Toronto, Toronto, Ontario, M6A 2E1, Canada
Luise Poustka
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany
Sarah Hohmann
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany
Juliane H. Fröhner
Affiliation:
Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
Michael N. Smolka
Affiliation:
Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
Henrik Walter
Affiliation:
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
Affiliation:
School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland
Gunter Schumann*
Affiliation:
Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King's College London, London, UK PONS Research Group, Department of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University, Berlin, Germany Leibniz Institute for Neurobiology, Magdeburg, Germany Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, P.R. China
Tianzi Jiang*
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Automation, Chinese Academy of Sciences, 95 East Zhongguancun Road, Beijing, 100190, China University of Chinese Academy of Sciences, 19 Yuquan Road, Beijing, 100049, China The Queensland Brain Institute, University of Queensland, Brisbane, QLD 4072, Australia
*
Authors for correspondence: Gunter Schumann, E-mail: gunter.schumann@kcl.ac.uk; Tianzi Jiang, E-mail: jiangtz@nlpr.ia.ac.cn
Authors for correspondence: Gunter Schumann, E-mail: gunter.schumann@kcl.ac.uk; Tianzi Jiang, E-mail: jiangtz@nlpr.ia.ac.cn
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Abstract

Background

Tobacco smoking remains one of the leading causes of preventable illness and death and is heritable with complex underpinnings. Converging evidence suggests a contribution of the polygenic risk for smoking to the use of tobacco and other substances. Yet, the underlying brain mechanisms between the genetic risk and tobacco smoking remain poorly understood.

Methods

Genomic, neuroimaging, and self-report data were acquired from a large cohort of adolescents from the IMAGEN study (a European multicenter study). Polygenic risk scores (PGRS) for smoking were calculated based on a genome-wide association study meta-analysis conducted by the Tobacco and Genetics Consortium. We examined the interrelationships among the genetic risk for smoking initiation, brain structure, and the number of occasions of tobacco use.

Results

A higher smoking PGRS was significantly associated with both an increased number of occasions of tobacco use and smaller cortical volume of the right orbitofrontal cortex (OFC). Furthermore, reduced cortical volume within this cluster correlated with greater tobacco use. A subsequent path analysis suggested that the cortical volume within this cluster partially mediated the association between the genetic risk for smoking and the number of occasions of tobacco use.

Conclusions

Our data provide the first evidence for the involvement of the OFC in the relationship between smoking PGRS and tobacco use. Future studies of the molecular mechanisms underlying tobacco smoking should consider the mediation effect of the related neural structure.

Keywords

Cortical volumeorbitofrontal cortexpolygenic risk scoresmokingtobacco use
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 6 , April 2022 , pp. 1175 - 1182
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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Footnotes

*

A list of authors and affiliations for the IMAGEN Consortium appears in the Supplementary note.

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