Adolescent binge drinking disrupts normal trajectories of brain functional organization and personality maturation

Hongtao Ruan; Yunyi Zhou; Qiang Luo; Gabriel H Robert; Sylvane Desrivières; Erin Burke Quinlan; ZhaoWen Liu; Tobias Banaschewski; Arun L W Bokde; Uli Bromberg; Christian Büchel; Herta Flor; Vincent Frouin; Hugh Garavan; Penny Gowland; Andreas Heinz; Bernd Ittermann; Jean-Luc Martinot; Marie-Laure Paillère Martinot; Frauke Nees; Dimitri Papadopoulos Orfanos; Luise Poustka; Sarah Hohmann; Juliane H Fröhner; Michael N Smolka; Henrik Walter; Robert Whelan; Fei Li; Gunter Schumann; Jianfeng Feng; IMAGEN Consortium

doi:10.1016/j.nicl.2019.101804

Adolescent binge drinking disrupts normal trajectories of brain functional organization and personality maturation

Neuroimage Clin. 2019:22:101804. doi: 10.1016/j.nicl.2019.101804. Epub 2019 Mar 31.

Authors

Hongtao Ruan¹, Yunyi Zhou¹, Qiang Luo², Gabriel H Robert³, Sylvane Desrivières⁴, Erin Burke Quinlan⁴, ZhaoWen Liu⁵, Tobias Banaschewski⁶, Arun L W Bokde⁷, Uli Bromberg⁸, Christian Büchel⁸, Herta Flor⁹, Vincent Frouin¹⁰, Hugh Garavan¹¹, Penny Gowland¹², Andreas Heinz¹³, Bernd Ittermann¹⁴, Jean-Luc Martinot¹⁵, Marie-Laure Paillère Martinot¹⁶, Frauke Nees¹⁷, Dimitri Papadopoulos Orfanos¹⁰, Luise Poustka¹⁸, Sarah Hohmann⁶, Juliane H Fröhner¹⁹, Michael N Smolka¹⁹, Henrik Walter¹³, Robert Whelan²⁰, Fei Li²¹, Gunter Schumann⁴, Jianfeng Feng²²; IMAGEN Consortium

Affiliations

¹ School of Mathematical Sciences, Fudan University, Shanghai 200433, PR China; Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, PR China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, PR China.
² Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, PR China; Department of Psychology and the Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge CB2 3EB, UK; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, PR China. Electronic address: qluo@fudan.edu.cn.
³ EA 4712 "Behavior and Basal Ganglia", Rennes University 1, Rennes, France.
⁴ Centre for Population Neuroscience and Stratified Medicine (PONS), Institute of Psychiatry, Psychology and Neuroscience, Social, Genetic and Developmental Psychiatry Centre, King's College London, London SE5 8AF, United Kingdom.
⁵ School of Computer Science and Technology, Xidian University, Xi'an 710071, Shannxi, PR China.
⁶ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany.
⁷ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Ireland.
⁸ University Medical Centre Hamburg-Eppendorf, House W34, 3.OG, Martinistr. 52, 20246, Hamburg, Germany.
⁹ Department 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.
¹⁰ NeuroSpin, CEA, Université Paris-Saclay, F-91191 Gif-sur-Yvette, France.
¹¹ Departments of Psychiatry and Psychology, University of Vermont, 05405 Burlington, VT, USA.
¹² Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.
¹³ Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charitéplatz 1, Berlin, Germany.
¹⁴ Physikalisch-Technische Bundesanstalt (PTB), Braunschweig, Abbestr. 2 - 12, Berlin, Germany.
¹⁵ Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging & Psychiatry", University Paris Sud, University Paris Descartes - Sorbonne Paris Cité; and Maison de Solenn, Paris, France.
¹⁶ Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging & Psychiatry", University Paris Sud, University Paris Descartes; Sorbonne Université; and AP-HP, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
¹⁷ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany; Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany.
¹⁸ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075 Göttingen, Germany.
¹⁹ Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
²⁰ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Ireland.
²¹ Developmental and Behavioral Pediatric Department & Child Primary Care Department, MOE-Shanghai Key Lab for Children's Environmental Health, Xinhua Hospital Affiliated To Shang Jiaotong University School of Medicine, Shanghai, PR China.
²² School of Mathematical Sciences, Fudan University, Shanghai 200433, PR China; Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, PR China; Department of Computer Science, University of Warwick, Coventry, UK; Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, PR China; Shanghai Center for Mathematical Sciences, Shanghai, PR China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, PR China.

Abstract

Adolescent binge drinking has been associated with higher risks for the development of many health problems throughout the lifespan. Adolescents undergo multiple changes that involve the co-development processes of brain, personality and behavior; therefore, certain behavior, such as alcohol consumption, can have disruptive effects on both brain development and personality maturation. However, these effects remain unclear due to the scarcity of longitudinal studies. In the current study, we used multivariate approaches to explore discriminative features in brain functional architecture, personality traits, and genetic variants in 19-year-old individuals (n = 212). Taking advantage of a longitudinal design, we selected features that were more drastically altered in drinkers with an earlier onset of binge drinking. With the selected features, we trained a hierarchical model of support vector machines using a training sample (n = 139). Using an independent sample (n = 73), we tested the model and achieved a classification accuracy of 71.2%. We demonstrated longitudinally that after the onset of binge drinking the developmental trajectory of improvement in impulsivity slowed down. This study identified the disrupting effects of adolescent binge drinking on the developmental trajectories of both brain and personality.

Keywords: Adolescent; Binge drinking; Co-development; Genome; Personality; Resting state.

Publication types

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

MeSH terms

Adolescent
Adolescent Development / physiology*
Adult
Age of Onset
Binge Drinking / diagnostic imaging
Binge Drinking / physiopathology*
Brain / diagnostic imaging
Brain / physiopathology*
Connectome / methods*
Female
Humans
Impulsive Behavior / physiology*
Longitudinal Studies
Magnetic Resonance Imaging
Male
Personality Development*
Support Vector Machine*
Time Factors
Underage Drinking*
Young Adult

Grants and funding

MR/N000390/1/MRC_/Medical Research Council/United Kingdom