Journal Article

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

Zhao, Qi, Whelan, Robert, Luo, Qiang, Quinlan, Erin B., Nees, Frauke, Martinot, Jean-Luc, Hohmann, Sarah, Büchel, Christian, Huang, Chu-Chung, Smolka, Michael N., Garavan, Hugh, Ittermann, Bernd, Heinz, Andreas, Flor, Herta, Banaschewski, Tobias, Frouin, Vincent, Orfanos, Dimitri Papadopoulos, Jia, Tianye, Martinot, Marie-Laure Paillère, Desrivières, Sylvane, Bokde, Arun L. W., Zheng, Yan, Gowland, Penny, Robbins, Trevor W., Poustka, Luise, Yao, Ye, Kanen, Jonathan W., Schumann, Gunter, Zhang, Lingli, Walter, Henrik, Feng, Jianfeng, Bromberg, Uli, Fröhner, Juliane H., Sahakian, Barbara J., Li, Fei

2020

Overview

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.

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: Abuse / Adolescent / Adult / Adult obesity / Adults / Age / Biobanks / Biomedicine / Body fat / Body mass / Body Mass Index / Body size / Body weight gain / Brain - pathology / Child abuse / Child Abuse - psychology / Childhood / Childhood trauma / Children / Cognition / Cognitive ability / Confidence intervals / Connectivity analysis / Control systems / Data collection / Drug use / Eating behavior / Female / Females / Genetic Predisposition to Disease / Humans / Hypothalamus / Hypothalamus (lateral) / Longitudinal Studies / Magnetic resonance imaging / Male / Medical imaging / Medicine / Medicine & Public Health / Morphometry / Neural networks / Neurocognitive control pathway / Neuroimaging / Obesity / Obesity - etiology / Overweight / Regression analysis / Research Article / Structural brain imaging / Subdivisions / Substantia alba / Substrates / Surveys and Questionnaires / Tensors / Trauma / Weight control / Weight Gain - physiology / Young Adult