Association between vmPFC gray matter volume and smoking initiation in adolescents

IMAGEN Consortium; 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

doi:10.1038/s41467-023-40079-2

Association between vmPFC gray matter volume and smoking initiation in adolescents

IMAGEN Consortium, 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 PoustkaSarah 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^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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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.

Original language	English
Article number	4684
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-40079-2
Publication status	Published - 15 Aug 2023

Keywords

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

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41467-023-40079-2Licence: CC BY

s41467-023-40079-2Final published version, 33.6 MBLicence: CC BY

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IMAGEN Consortium, Xiang, S., Jia, T., Xie, C., Cheng, W., Chaarani, B., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Büchel, C., Desrivières, S., Flor, H., Grigis, A., Gowland, P. A., Brühl, R., Martinot, J.-L., Martinot, M.-L. P., Nees, F., Orfanos, D. P., ... Feng, J. (2023). Association between vmPFC gray matter volume and smoking initiation in adolescents. Nature Communications, 14(1), Article 4684. https://doi.org/10.1038/s41467-023-40079-2

@article{cd407f72854e49d982dfc3c785ad4ab4,

title = "Association between vmPFC gray matter volume and smoking initiation in adolescents",

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.",

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

author = "{IMAGEN Consortium} and Shitong Xiang and Tianye Jia and Chao Xie and Wei Cheng and Bader Chaarani and Tobias Banaschewski and Barker, {Gareth J} and Bokde, {Arun L W} and Christian B{\"u}chel and Sylvane Desrivi{\`e}res and Herta Flor and Antoine Grigis and Gowland, {Penny A} and R{\"u}diger Br{\"u}hl and Jean-Luc Martinot and Martinot, {Marie-Laure Paill{\`e}re} and Frauke Nees and Orfanos, {Dimitri Papadopoulos} and Luise Poustka and Sarah Hohmann and Fr{\"o}hner, {Juliane H} and Smolka, {Michael N} and Nilakshi Vaidya and Henrik Walter and Robert Whelan and Hugh Garavan and Gunter Schumann and Sahakian, {Barbara J} and Robbins, {Trevor W} and Jianfeng Feng",

note = "Funding Information: We thank Professor David Nutt and Professor Stephan Ripke for their helpful comments on the manuscript. We thank the IMAGEN Consortium for providing the discover data. This work received support from the following sources: National Key R and D Program of China (2021YFC2501402 [to T.J.], 2022CSJGG1000 [to T.J.], 2019YFA0709501 [to T.J.], 2019YFA0709502 [to J.F.], 2018YFC1312900 [to T.J.] and 2018YFC1312904 [to J.F.]), the National Natural Science Foundation of China (T2122005 [to T.J.], 82150710554 [to G.S.] and 81801773 [to T.J.]), the Shanghai Pujiang Project (18PJ1400900 [to T.J.]), Guangdong Key Research and Development Project (2018B030335001 [to J.F.]), the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT- 2007-037286 [to G.S.]), the 111 Project (B18015 [to J.F.]), the key project of Shanghai Science and Technology (16JC1420402 [to J.F.]), Shanghai Municipal Science and Technology Major Project (2018SHZDZX01 [to J.F.]), Zhangjiang Lab [to J.F.], Shanghai Center for Brain Science and Brain-Inspired Technology [to J.F.], the European Research Area Network on Illicit Drugs (ERANID) (Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways, PR-ST-0416-10004 [to G.S.]), Human Brain Project (HBP SGA 2, 785907, and HBP SGA 3, 945539 [to G.S.]), the Medical Research Council Grant {\textquoteleft}c-VEDA{\textquoteright} (Consortium on Vulnerability to Externalizing Disorders and Addictions, MR/N000390/1 [to G.S.]), the National Institute of Health (NIH) (A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers, R01DA049238 [to G.S.]), the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King{\textquoteright}s College London, the Bundesministeriumf{\"u}r Bildung und Forschung (BMBF grants 01GS08152; 01EV0711 [to G.S.]; the European Union and UKRI funded project {\textquoteleft}environMENTAL{\textquoteright} (grants 101057429 [to G.S.] and 10038599 [to S.D.]); Forschungsnetz AERIAL 01EE1406A, 01EE1406B and Forschungsnetz IMAC-Mind 01GL1745B [to G.S.]), the Medical Research Foundation and Medical Research Council (grants MR/R00465X/1, MR/S020306/1 and MRF-058-0009-RG-DESR-C0759 [to S.D.]), the National Institutes of Health (NIH) funded ENIGMA (grants 5U54EB020403-05 and 1R56AG058854-01 [to S.D.]). Further support was provided by grants from: - the ANR (ANR-12-SAMA-0004 [to M.-L.P.M.], AAPG2019 – GeBra [to J.-L.M.]), the Eranet Neuron (AF12-NEUR0008-01 - WM2NA; and ANR-18-NEUR00002-01 – ADORe [to J.-L.M.]), the Fondation de France (00081242 [to J.-L.M.]), the Fondation pour la Recherche M{\'e}dicale (DPA20140629802 [to J.-L.M.]), the Mission Interminist{\'e}rielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA [to J.-L.M.]), the Assistance-Publique-H{\^o}pitaux-de-Paris and INSERM (interface grant [to M.-L.P.M.]), Paris Sud University IDEX 2012 [to J.-L.M.], the Fondation de l{\textquoteright}Avenir (grant AP-RM-17-013 [to M.-L.P.M.]), the F{\'e}d{\'e}ration pour la Recherche sur le Cerveau; the National Institutes of Health, Science Foundation Ireland (16/ERCD/3797 [to R.W.]). The views expressed in this article are those of the authors and not necessarily those of the national funding agencies or ERANID. Publisher Copyright: {\textcopyright} 2023, Springer Nature Limited.",

year = "2023",

month = aug,

day = "15",

doi = "10.1038/s41467-023-40079-2",

language = "English",

volume = "14",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

IMAGEN Consortium, Xiang, S, Jia, T, Xie, C, Cheng, W, Chaarani, B, Banaschewski, T, Barker, GJ, Bokde, ALW, Büchel, C, Desrivières, S, Flor, H, Grigis, A, Gowland, PA, Brühl, R, Martinot, J-L, Martinot, M-LP, Nees, F, Orfanos, DP, Poustka, L, Hohmann, S, Fröhner, JH, Smolka, MN, Vaidya, N, Walter, H, Whelan, R, Garavan, H, Schumann, G, Sahakian, BJ, Robbins, TW & Feng, J 2023, 'Association between vmPFC gray matter volume and smoking initiation in adolescents', Nature Communications, vol. 14, no. 1, 4684. https://doi.org/10.1038/s41467-023-40079-2

TY - JOUR

T1 - Association between vmPFC gray matter volume and smoking initiation in adolescents

AU - IMAGEN Consortium

AU - Xiang, Shitong

AU - Jia, Tianye

AU - Xie, Chao

AU - Cheng, Wei

AU - Chaarani, Bader

AU - Banaschewski, Tobias

AU - Barker, Gareth J

AU - Bokde, Arun L W

AU - Büchel, Christian

AU - Desrivières, Sylvane

AU - Flor, Herta

AU - Grigis, Antoine

AU - Gowland, Penny A

AU - Brühl, Rüdiger

AU - Martinot, Jean-Luc

AU - Martinot, Marie-Laure Paillère

AU - Nees, Frauke

AU - Orfanos, Dimitri Papadopoulos

AU - Poustka, Luise

AU - Hohmann, Sarah

AU - Fröhner, Juliane H

AU - Smolka, Michael N

AU - Vaidya, Nilakshi

AU - Walter, Henrik

AU - Whelan, Robert

AU - Garavan, Hugh

AU - Schumann, Gunter

AU - Sahakian, Barbara J

AU - Robbins, Trevor W

AU - Feng, Jianfeng

N1 - Funding Information: We thank Professor David Nutt and Professor Stephan Ripke for their helpful comments on the manuscript. We thank the IMAGEN Consortium for providing the discover data. This work received support from the following sources: National Key R and D Program of China (2021YFC2501402 [to T.J.], 2022CSJGG1000 [to T.J.], 2019YFA0709501 [to T.J.], 2019YFA0709502 [to J.F.], 2018YFC1312900 [to T.J.] and 2018YFC1312904 [to J.F.]), the National Natural Science Foundation of China (T2122005 [to T.J.], 82150710554 [to G.S.] and 81801773 [to T.J.]), the Shanghai Pujiang Project (18PJ1400900 [to T.J.]), Guangdong Key Research and Development Project (2018B030335001 [to J.F.]), the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT- 2007-037286 [to G.S.]), the 111 Project (B18015 [to J.F.]), the key project of Shanghai Science and Technology (16JC1420402 [to J.F.]), Shanghai Municipal Science and Technology Major Project (2018SHZDZX01 [to J.F.]), Zhangjiang Lab [to J.F.], Shanghai Center for Brain Science and Brain-Inspired Technology [to J.F.], the European Research Area Network on Illicit Drugs (ERANID) (Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways, PR-ST-0416-10004 [to G.S.]), Human Brain Project (HBP SGA 2, 785907, and HBP SGA 3, 945539 [to G.S.]), the Medical Research Council Grant ‘c-VEDA’ (Consortium on Vulnerability to Externalizing Disorders and Addictions, MR/N000390/1 [to G.S.]), the National Institute of Health (NIH) (A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers, R01DA049238 [to G.S.]), the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, the Bundesministeriumfür Bildung und Forschung (BMBF grants 01GS08152; 01EV0711 [to G.S.]; the European Union and UKRI funded project ‘environMENTAL’ (grants 101057429 [to G.S.] and 10038599 [to S.D.]); Forschungsnetz AERIAL 01EE1406A, 01EE1406B and Forschungsnetz IMAC-Mind 01GL1745B [to G.S.]), the Medical Research Foundation and Medical Research Council (grants MR/R00465X/1, MR/S020306/1 and MRF-058-0009-RG-DESR-C0759 [to S.D.]), the National Institutes of Health (NIH) funded ENIGMA (grants 5U54EB020403-05 and 1R56AG058854-01 [to S.D.]). Further support was provided by grants from: - the ANR (ANR-12-SAMA-0004 [to M.-L.P.M.], AAPG2019 – GeBra [to J.-L.M.]), the Eranet Neuron (AF12-NEUR0008-01 - WM2NA; and ANR-18-NEUR00002-01 – ADORe [to J.-L.M.]), the Fondation de France (00081242 [to J.-L.M.]), the Fondation pour la Recherche Médicale (DPA20140629802 [to J.-L.M.]), the Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA [to J.-L.M.]), the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant [to M.-L.P.M.]), Paris Sud University IDEX 2012 [to J.-L.M.], the Fondation de l’Avenir (grant AP-RM-17-013 [to M.-L.P.M.]), the Fédération pour la Recherche sur le Cerveau; the National Institutes of Health, Science Foundation Ireland (16/ERCD/3797 [to R.W.]). The views expressed in this article are those of the authors and not necessarily those of the national funding agencies or ERANID. Publisher Copyright: © 2023, Springer Nature Limited.

PY - 2023/8/15

Y1 - 2023/8/15

N2 - 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.

AB - 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.

KW - Humans

KW - Adolescent

KW - Gray Matter/diagnostic imaging

KW - Magnetic Resonance Imaging/methods

KW - Prefrontal Cortex/diagnostic imaging

KW - Smoking/adverse effects

KW - Tobacco Use Disorder

KW - Brain

UR - http://www.scopus.com/inward/record.url?scp=85168059631&partnerID=8YFLogxK

U2 - 10.1038/s41467-023-40079-2

DO - 10.1038/s41467-023-40079-2

M3 - Article

C2 - 37582920

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4684

ER -

Association between vmPFC gray matter volume and smoking initiation in adolescents

Abstract

Keywords

UN SDGs

Access to Document

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environMENTA: Reducing the impact of major environmental challenges on mental health

Human Brain Project Specific Grant Agreement 3

A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers

Cite this

Association between vmPFC gray matter volume and smoking initiation in adolescents

Abstract

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Projects

environMENTA: Reducing the impact of major environmental challenges on mental health

Human Brain Project Specific Grant Agreement 3

A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers

Cite this