Neural correlates of the volitional regulation of the desire for food

Abstract

Objective: In this study, we investigate the brain mechanisms of the conscious regulation of the desire for food using functional magnetic resonance imaging. Further, we examine associations between hemodynamic responses and participants' cognitive restraint of eating (CRE), as well as their susceptibility to uncontrolled eating. Subjects: Seventeen non-vegetarian, right-handed, female Caucasian participants (age: 20-30 years, mean 25.3 years±3.1 s.d.; BMI: 20.2-31.2 kg m À2 , mean 25.1 ± 3.5 s.d.). Measurements: During scanning, our participants viewed pictures of food items they had pre-rated according to tastiness and healthiness. Participants were either allowed to admit to the desire for the food (ADMIT) or they were instructed to downregulate their desire using a cognitive reappraisal strategy, that is, thinking of negative long-term health-related and social consequences (REGULATE).Results: Comparing the hemodynamic responses of the REGULATE with the ADMIT condition, we observed robust activation in the dorsolateral prefrontal cortex (DLPFC), the pre-supplementary motor area, the inferior frontal gyrus (IFG), the dorsal striatum (DS), the bilateral orbitofrontal cortex (OFC), the anterior insula and the temporo-parietal junction (TPJ). Activation in the DLPFC and the DS strongly correlated with the degree of dietary restraint under both conditions. Conclusion: Cortical activation in the DLPFC, the pre-supplementary motor area and the inferior frontal gyrus (IFG) are known to underpin top-down control, inhibition of learned associations and pre-potent responses. The observed hemodynamic responses in the lateral OFC, the DS, the anterior insula and the TPJ support the notion of reward valuation and integration, interoceptive awareness, and self-reflection as key processes during active regulation of desire for food. In conclusion, an active reappraisal of unhealthy food recruits the brain's valuation system in combination with prefrontal cognitive control areas associated with response inhibition. The correlations between brain responses and CRE suggest that individuals with increased cognitive restraint show an automatic predisposition to regulate the hedonic aspects of food stimuli. This cognitive control might be necessary to counterbalance a lack of homeostatic mechanisms.

The potential role of and deficits in frontal cortical brain areas implicated in executive control of food intake

“…13 The observation of a similar lack of post-meal cortical brain activity related to inhibition of further eating in the PWS subjects suggests indeed that PWS may be an extreme model of obesity. The observations by Hollman et al 3 also confirm earlier observations on the contribution of cortical brain activationrelated ability to inhibit food intake and thereby energy intake. [13][14][15][16][17][18][19] Interestingly, the observations related to obesity, PWS, as well as to dietary restraint, fit well with the suggested bell-shaped reward-addiction-reward-deficiency model.…”

“…On the other hand, Hollman et al 3 showed a greater cortical activation in the cognitive-restrained subjects, related to predisposition to control food intake, especially the hedonic effects of it. 3 Rather puzzling are the observations by Frankort et al, 4 introducing diverting effects to pictures of foods that are high or low calorie and have a range in palatability.…”

“…On the other hand, Hollman et al 3 showed a greater cortical activation in the cognitive-restrained subjects, related to predisposition to control food intake, especially the hedonic effects of it. 3 Rather puzzling are the observations by Frankort et al, 4 introducing diverting effects to pictures of foods that are high or low calorie and have a range in palatability. The observations described in the first two papers partly confirm previous observations, [5][6][7][8][9][10][11] that in addition have shown that effects may depend on the severity of obesity, age and sex, leading to the hypothesis that low GM volumes and high WM volumes increase the risk for obesity.…”

“…The data are interpreted to support the view that an active reappraisal of an unhealthy food recruits brain valuation systems in combination with prefrontal control areas associated with response inhibition, and that individuals with high levels of cognitive restraint show an automatic predisposition to regulate hedonic aspects of feeding. 3 Finally, Frankort et al 4 report data from a study examining how attention affects reward-related brain activity in satiated overweight and normal weight in response to high-calorie palatable food pictures. They compared patterns of neural activity in response to the pictures when subjects were either not given any instructions or when they were asked to imagine the taste of the food item.…”

“…Thus, in PWS there is dysfunction in dual circuits involved in food reward and decision-making processes regarding food intake, and that the lack of normal cortical activation following a meal in PWS may contribute to their satiety deficits. 2 As a response to this apparently diminished control over food intake, Hollmann et al 3 report on a study in healthy volunteers designed to examine how instructions to either admit to a desire for food or to actively try to downregulate that desire using a cognitive reappraisal strategy affected patterns of neural activation when shown food items that had been rated for their tastiness and healthiness. The data demonstrate that, under the downregulation condition, there was greater activation in prefrontal-control-related brain areas and in cortical and subcortical regions involved in reward valuation and interoceptive signaling.…”