Spatiotemporal profile of altered neural reactivity to food images in obesity: Reward system is altered automatically and predicts efficacy of weight loss intervention.

Abstract

Obesity presents a significant public health problem. Brain plays a central role in etiology and maintenance of obesity. Prior neuroimaging studies have found that individuals with obesity exhibit altered neural responses to images of food within the brain reward system and related brain networks. However, little is known about the dynamics of these neural responses or their relationship to later weight change. In particular, it is unknown if in obesity, the altered reward response to food images emerges early and automatically, or later, in the controlled stage of processing. It also remains unclear if the pretreatment reward system reactivity to food images is predictive of subsequent weight loss intervention outcome. In this study, we presented high-calorie and low-calorie food, and nonfood images to individuals with obesity, who were then prescribed lifestyle changes, and matched normal-weight controls, and examined neural reactivity using magnetoencephalography (MEG). We performed whole-brain analysis to explore and characterize large-scale dynamics of brain systems affected in obesity, and tested two specific hypotheses: (1) in obese individuals, the altered reward system reactivity to food images occurs early and automatically, and (2) pretreatment reward system reactivity predicts the outcome of lifestyle weight loss intervention, with reduced activity associated with successful weight loss. We identified a distributed set of brain regions and their precise temporal dynamics that showed altered response patterns in obesity. Specifically, we found reduced neural reactivity to food images in brain networks of reward and cognitive control, and elevated reactivity in regions of attentional control and visual processing. The hypoactivity in reward system emerged early, in the automatic stage of processing (< 150 ms post-stimulus). Reduced reward and attention responsivity, and elevated neural cognitive control were predictive of weight loss after six months in treatment. In summary, we have identified, for the first time with high temporal resolution, the large-scale dynamics of brain reactivity to food images in obese versus normal-weight individuals, and have confirmed both our hypotheses. These findings have important implications for our understanding of neurocognition and eating behavior in obesity, and can facilitate development of novel integrated treatment strategies, including tailored cognitive-behavioral and pharmacological therapies.