Qiang Luo, Tobias Banaschewski, Juliane H. Fröhner, Trevor W. Robbins, Chu Chung Huang, Christian Büchel, Qi Zhao, Sarah Hohmann, Herta Flor, Gunter Schumann, Michael N. Smolka, Barbara J. Sahakian, Luise Poustka, Erin Burke Quinlan, Yan Zheng, Marie-Laure Paillère Martinot, Jianfeng Feng, Lingli Zhang, Frauke Nees, Uli Bromberg, Hugh Garavan, Jonathan W. Kanen, Jean-Luc Martinot, Dimitri Papadopoulos Orfanos, Penny A. Gowland, Sylvane Desrivières, Arun L.W. Bokde, Fei Li, Tianye Jia, Bernd Ittermann, Henrik Walter, Vincent Frouin, Ye Yao, Robert Whelan, Andreas Heinz, Apollo - University of Cambridge Repository, Sahakian, Barbara [0000-0001-7352-1745], and Robbins, Trevor [0000-0003-0642-5977]
Funder: Zhangjiang Lab, Funder: the Shanghai AI Platform for Diagnosis and Treatment of Brain Diseases, Funder: the Project of Zhangjiang Hi-Tech District Management Committee, Funder: Shanghai (grant 2016-17), Funder: BRIDGET (JPND: BRain Imaging, cognition Dementia and next generation GEnomics); Grant(s): MR/N027558/1, Funder: Associazione Emma e Ernesto Rulfo per la Genetica Medica (IT), Funder: the Swedish Research Council FORMAS, Funder: the Medical Research Council, Funder: the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, Funder: the Human Brain Project (HBP SGA 2), Funder: the Fondation de France, the Fondation pour la Recherche Médicale, Funder: the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Funder: Paris Sud University IDEX 2012, Funder: cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence, 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.