Association between childhood trauma and risk for obesity: a putative neurocognitive developmental pathway

BMC Medicine

Tobias Banaschewski¹  Sarah Hohmann¹  Frauke Nees²  Luise Poustka³  Herta Flor⁴  Michael N. Smolka⁵  Juliane H. Fröhner⁵  Andreas Heinz⁶  Henrik Walter⁶  Jonathan W. Kanen⁷  Hugh Garavan⁸  Lingli Zhang⁹  Fei Li⁹  Arun L. W. Bokde^1,10  Marie-Laure Paillère Martinot^1,11  Jean-Luc Martinot^1,12  Chu-Chung Huang^1,13  Ye Yao^1,13  Qi Zhao^1,13  Jianfeng Feng^1,14  Trevor W. Robbins^1,15  Barbara J. Sahakian^1,16  Qiang Luo^1,17  Tianye Jia^1,18  Gunter Schumann^1,18  Erin B. Quinlan^1,19  Sylvane Desrivières^1,19  Vincent Frouin^2,20  Dimitri Papadopoulos Orfanos^2,20  Bernd Ittermann^2,21  Robert Whelan^2,22  Penny Gowland^2,23  Yan Zheng^2,24  Christian Büchel^2,25  Uli Bromberg^2,25 

[1] Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany;Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany;Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany;Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, Göttingen, Germany;Clinic for Child and Adolescent Psychiatry, Medical University of Vienna, Währinger Gürtel, Vienna, Austria;Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany;Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany;Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany;Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin, Germany;Departments of Psychiatry and Psychology and the Behavioural and Clinical Neuroscience Institute, University of Cambridge, CB2 3EB, Cambridge, UK;Departments of Psychiatry and Psychology, University of Vermont, Burlington, USA;Developmental and Behavioral Pediatric Department & Child Primary Care Department, Ministry of Education Key Laboratory for Children’s Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092, Shanghai, People’s Republic of China;Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland;Institute National de la Santé et de la Recherche Médicale Unit 1000, Neuroimaging and Psychiatry, University Paris Sud–Paris Saclay, University Paris Descartes, Paris, France;Assistance Publique–Hôpitaux de Paris, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France;Institute National de la Santé et de la Recherche Médicale Unit 1000, Neuroimaging and Psychiatry, University Paris Sud–Paris Saclay, University Paris Descartes, Paris, France;Service Hospitalier Frédéric Joliot, Orsay, France;Maison de Solenn, Paris, France;Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, 200433, Shanghai, People’s Republic of China;Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, 200433, Shanghai, People’s Republic of China;Department of Computer Science, University of Warwick, Coventry, UK;Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, People’s Republic of China;Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, 200433, Shanghai, People’s Republic of China;Departments of Psychiatry and Psychology and the Behavioural and Clinical Neuroscience Institute, University of Cambridge, CB2 3EB, Cambridge, UK;Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, 200433, Shanghai, People’s Republic of China;Developmental and Behavioral Pediatric Department & Child Primary Care Department, Ministry of Education Key Laboratory for Children’s Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092, Shanghai, People’s Republic of China;Departments of Psychiatry and Psychology and the Behavioural and Clinical Neuroscience Institute, University of Cambridge, CB2 3EB, Cambridge, UK;Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, 200433, Shanghai, People’s Republic of China;Developmental and Behavioral Pediatric Department & Child Primary Care Department, Ministry of Education Key Laboratory for Children’s Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092, Shanghai, People’s Republic of China;State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Institutes of Brain Science and Human Phenome Institute, Fudan University, 200433, Shanghai, People’s Republic of China;Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, 200433, Shanghai, People’s Republic of China;Medical Research Council - Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, SE5 8AF, London, UK;Medical Research Council - Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, SE5 8AF, London, UK;NeuroSpin, Commissariat à L’énergie Atomique, Université Paris-Saclay, Gif-sur-Yvette, France;Physikalisch-Technische Bundesanstalt (PTB), Abbestr. 2-12, Berlin, Germany;School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland;Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, UK;State Key Laboratory of Genetic Engineering, School of Life Sciences, Human Phenome Institute, Zhongshan Hospital, Fudan University, 2005 Songhu Road, 200438, Shanghai, People’s Republic of China;University Medical Centre Hamburg-Eppendorf, Hamburg, Germany;

关键词: Childhood trauma;    Adult obesity;    Neurocognitive control pathway;    Structural brain imaging;   

DOI  :  10.1186/s12916-020-01743-2

来源: Springer

【 摘 要 】

BackgroundChildhood trauma increases the risk for adult obesity through multiple complex pathways, and the neural substrates are yet to be determined.MethodsParticipants from three population-based neuroimaging cohorts, including the IMAGEN cohort, the UK Biobank (UKB), and the Human Connectome Project (HCP), were recruited. Voxel-based morphometry analysis of both childhood trauma and body mass index (BMI) was performed in the longitudinal IMAGEN cohort; validation of the findings was performed in the UKB. White-matter connectivity analysis was conducted to study the structural connectivity between the identified brain region and subdivisions of the hypothalamus in the HCP.ResultsIn IMAGEN, a smaller frontopolar cortex (FPC) was associated with both childhood abuse (CA) (β = − .568, 95%CI − .942 to − .194; p = .003) and higher BMI (β = − .086, 95%CI − .128 to − .043; p < .001) in male participants, and these findings were validated in UKB. Across seven data collection sites, a stronger negative CA-FPC association was correlated with a higher positive CA-BMI association (β = − 1.033, 95%CI − 1.762 to − .305; p = .015). Using 7-T diffusion tensor imaging data (n = 156), we found that FPC was the third most connected cortical area with the hypothalamus, especially the lateral hypothalamus. A smaller FPC at age 14 contributed to higher BMI at age 19 in those male participants with a history of CA, and the CA-FPC interaction enabled a model at age 14 to account for some future weight gain during a 5-year follow-up (variance explained 5.8%).ConclusionsThe findings highlight that a malfunctioning, top-down cognitive or behavioral control system, independent of genetic predisposition, putatively contributes to excessive weight gain in a particularly vulnerable population, and may inform treatment approaches.

【 授权许可】

CC BY