Association between vmPFC gray matter volume and smoking initiation in adolescents

Shitong Xiang; Tianye Jia; Chao Xie; Wei Cheng; Bader Chaarani; Tobias Banaschewski; Gareth J Barker; Arun L W Bokde; Christian Büchel; Sylvane Desrivières; Herta Flor; Antoine Grigis; Penny A Gowland; Rüdiger Brühl; Jean-Luc Martinot; Marie-Laure Paillère Martinot; Frauke Nees; Dimitri Papadopoulos Orfanos; Luise Poustka; Sarah Hohmann; Juliane H Fröhner; Michael N Smolka; Nilakshi Vaidya; Henrik Walter; Robert Whelan; Hugh Garavan; Gunter Schumann; Barbara J Sahakian; Trevor W Robbins; Jianfeng Feng; IMAGEN Consortium

doi:10.1038/s41467-023-40079-2

Association between vmPFC gray matter volume and smoking initiation in adolescents

Nat Commun. 2023 Aug 15;14(1):4684. doi: 10.1038/s41467-023-40079-2.

Authors

Shitong Xiang^#^{1

2}, Tianye Jia^#^{3

4

5

6}, Chao Xie^{1

2}, Wei Cheng^{1

2}, Bader Chaarani⁷, Tobias Banaschewski⁸, Gareth J Barker⁹, Arun L W Bokde¹⁰, Christian Büchel¹¹, Sylvane Desrivières¹², Herta Flor^{13

14}, Antoine Grigis¹⁵, Penny A Gowland¹⁶, Rüdiger Brühl¹⁷, Jean-Luc Martinot¹⁸, Marie-Laure Paillère Martinot^{18

19}, Frauke Nees^{8

13

20}, Dimitri Papadopoulos Orfanos¹⁴, Luise Poustka²¹, Sarah Hohmann⁸, Juliane H Fröhner²², Michael N Smolka²², Nilakshi Vaidya²³, Henrik Walter²³, Robert Whelan²⁴, Hugh Garavan⁷, Gunter Schumann^{1

25

23

26}, Barbara J Sahakian^{1

27}, Trevor W Robbins^{28

29}, Jianfeng Feng^{30

31

32

33}; IMAGEN Consortium

Affiliations

¹ Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China.
² Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China.
³ Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China. [email protected].
⁴ Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China. [email protected].
⁵ Centre for Population Neuroscience and Stratified Medicine (PONS Centre), ISTBI, Fudan University, Shanghai, China. [email protected].
⁶ Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. [email protected].
⁷ Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, USA.
⁸ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁹ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹⁰ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
¹¹ University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
¹² Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹³ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹⁴ Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany.
¹⁵ NeuroSpin, C.E.A., Université Paris-Saclay, Gif-sur-Yvette, France.
¹⁶ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, UK.
¹⁷ Physikalisch-Technische Bundesanstalt (PTB), Berlin, Germany.
¹⁸ Institut National de la Santé et de la Recherche Médicale, INSERM U1299 'Trajectoires développementales en psychiatrie', Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS UMR9010, Centre Borelli, Gif-sur-Yvette, France.
¹⁹ AP-HP, Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
²⁰ Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany.
²¹ Department of Child and Adolescent Psychiatry, Center for Psychosocial Medicine, University Hospital Heidelberg, Heidelberg, Germany.
²² Department of Psychiatry and Psychotherapy, Technische Universität Dresden, Dresden, Germany.
²³ Department of Psychiatry and Neurosciences, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität BerlinHumboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
²⁴ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
²⁵ Centre for Population Neuroscience and Stratified Medicine (PONS Centre), ISTBI, Fudan University, Shanghai, China.
²⁶ Centre for Population Neuroscience and Stratified Medicine (PONS Centre), Charité University Medicine Berlin, Berlin, Germany.
²⁷ Department of Psychiatry and Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK.
²⁸ Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China. [email protected].
²⁹ Department of Psychology and Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK. [email protected].
³⁰ Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China. [email protected].
³¹ Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China. [email protected].
³² Department of Computer Science, University of Warwick, Coventry, United Kingdom. [email protected].
³³ Zhangjiang Fudan International Innovation Center, Shanghai, China. [email protected].

^# Contributed equally.

Abstract

Smoking of cigarettes among young adolescents is a pressing public health issue. However, the neural mechanisms underlying smoking initiation and sustenance during adolescence, especially the potential causal interactions between altered brain development and smoking behaviour, remain elusive. Here, using large longitudinal adolescence imaging genetic cohorts, we identify associations between left ventromedial prefrontal cortex (vmPFC) gray matter volume (GMV) and subsequent self-reported smoking initiation, and between right vmPFC GMV and the maintenance of smoking behaviour. Rule-breaking behaviour mediates the association between smaller left vmPFC GMV and smoking behaviour based on longitudinal cross-lagged analysis and Mendelian randomisation. In contrast, smoking behaviour associated longitudinal covariation of right vmPFC GMV and sensation seeking (especially hedonic experience) highlights a potential reward-based mechanism for sustaining addictive behaviour. Taken together, our findings reveal vmPFC GMV as a possible biomarker for the early stages of nicotine addiction, with implications for its prevention and treatment.

Publication types

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

MeSH terms

Adolescent
Brain
Gray Matter* / diagnostic imaging
Humans
Magnetic Resonance Imaging / methods
Prefrontal Cortex / diagnostic imaging
Smoking / adverse effects
Tobacco Use Disorder*

Abstract

Publication types

MeSH terms

Grants and funding