BMC Medicine (Oct 2020)
Association between childhood trauma and risk for obesity: a putative neurocognitive developmental pathway
- Qiang Luo,
- Lingli Zhang,
- Chu-Chung Huang,
- Yan Zheng,
- Jonathan W. Kanen,
- Qi Zhao,
- Ye Yao,
- Erin B. Quinlan,
- Tianye Jia,
- 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,
- Barbara J. Sahakian,
- Gunter Schumann,
- Fei Li,
- Jianfeng Feng,
- Sylvane Desrivières,
- Trevor W. Robbins,
- for the IMAGEN consortium
Affiliations
- Qiang Luo
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Lingli Zhang
- 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
- Chu-Chung Huang
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Yan Zheng
- State Key Laboratory of Genetic Engineering, School of Life Sciences, Human Phenome Institute, Zhongshan Hospital, Fudan University
- Jonathan W. Kanen
- Departments of Psychiatry and Psychology and the Behavioural and Clinical Neuroscience Institute, University of Cambridge
- Qi Zhao
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Ye Yao
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Erin B. Quinlan
- Medical Research Council - Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London
- Tianye Jia
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Tobias Banaschewski
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University
- Arun L. W. Bokde
- Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin
- Uli Bromberg
- University Medical Centre Hamburg-Eppendorf
- Christian Büchel
- University Medical Centre Hamburg-Eppendorf
- Herta Flor
- Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University
- Vincent Frouin
- NeuroSpin, Commissariat à L’énergie Atomique, Université Paris-Saclay
- Hugh Garavan
- Departments of Psychiatry and Psychology, University of Vermont
- Penny Gowland
- Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park
- Andreas Heinz
- Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin
- Bernd Ittermann
- Physikalisch-Technische Bundesanstalt (PTB)
- Jean-Luc Martinot
- Institute National de la Santé et de la Recherche Médicale Unit 1000, Neuroimaging and Psychiatry, University Paris Sud–Paris Saclay, University Paris Descartes
- Marie-Laure Paillère Martinot
- Institute National de la Santé et de la Recherche Médicale Unit 1000, Neuroimaging and Psychiatry, University Paris Sud–Paris Saclay, University Paris Descartes
- Frauke Nees
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University
- Dimitri Papadopoulos Orfanos
- NeuroSpin, Commissariat à L’énergie Atomique, Université Paris-Saclay
- Luise Poustka
- Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen
- Sarah Hohmann
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University
- Juliane H. Fröhner
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden
- Michael N. Smolka
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden
- Henrik Walter
- Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin
- Robert Whelan
- School of Psychology and Global Brain Health Institute, Trinity College Dublin
- Barbara J. Sahakian
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Gunter Schumann
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Fei Li
- 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
- Jianfeng Feng
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- Sylvane Desrivières
- Medical Research Council - Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London
- Trevor W. Robbins
- Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University
- for the IMAGEN consortium
- DOI
- https://doi.org/10.1186/s12916-020-01743-2
- Journal volume & issue
-
Vol. 18,
no. 1
pp. 1 – 14
Abstract
Abstract Background Childhood trauma increases the risk for adult obesity through multiple complex pathways, and the neural substrates are yet to be determined. Methods Participants 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. Results In 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%). Conclusions The 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.
Keywords