Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt

Abstract

Background: Obese compared with lean individuals show greater attention-, gustatory-, and reward-region responsivity to food cues but reduced reward-region responsivity during food intake. However, to our knowledge, research has not tested whether an objectively measured caloric intake is positively associated with neural responsivity independent of excess adipose tissue. Objective: We tested the hypothesis that objectively measured energy intake, which accounts for basal needs and the percentage of body fat, correlates positively with the neural response to anticipated palatable food intake but negatively with a response to food intake in healthy-weight adolescents. Design: Participants (n = 155; mean 6 SD age: 15.9 6 1.1 y) completed functional magnetic resonance imaging scans while anticipating and receiving palatable food compared with a tasteless solution, a doubly labeled water assessment of energy intake, and assessments of resting metabolic rate and body composition. Results: Energy intake correlated positively with activation in the lateral visual and anterior cingulate cortices (visual processing and attention), frontal operculum (primary gustatory cortex) when anticipating palatable food, and greater striatal activation when anticipating palatable food in a more-sensitive region of interest analysis. Energy intake was not significantly related to neural responsivity during palatable food intake. Conclusions: Results indicate that objectively measured energy intake that accounts for basal needs and adipose tissue correlates positively with activity in attentional, gustatory, and reward regions when anticipating palatable food. Although hyperresponsivity of these regions may increase risk of overeating, it is unclear whether this is an initial vulnerability factor or a result of previous overeating. This trial was registered at clinicaltrials.gov as NCT01807572.Am J Clin Nutr 2013;97:1188-94.

Frontostriatal and behavioral adaptations to daily sugar-sweetened beverage intake: a randomized controlled trial

“…For example, frequent ice cream consumption was related to a reduced striatal and prefrontal response during the receipt of milkshake in lean adolescents (22), a finding supported by additional reports (23,24). Furthermore, objective measures of elevated caloric intake have been shown to increase visual cortex and parietal response during cue-elicited anticipation of a palatable food (25). Last, regular Coke consumers have shown increased visual cortex and parietal response during exposure to Coke advertisements relative to their nonconsuming counterparts independent of weight status (26).…”

“…The precuneus, which is located in the parietal lobe, has been shown to increase during exposure to familiar relative to nonfamiliar brands and logos (26,42,43), which is in line with the notion that this region most commonly responds to emotionally salient stimuli independent of valance (44). Burger and Stice (22) observed a similar response pattern, in which the reduced striatal response to palatable food receipt was specified to the consumption of that food, when overeating, in general, was associated with an increased precuneus response to cue-elicited anticipation of palatable food receipt (25). Collectively, these reports and the results reported herein suggest that, in healthy-weight individuals, the reduced striatal response to food intake may be very specified to the foods repeatedly consumed, whereas increases to the precuneus response to anticipatory stimuli may be more generalized.…”

Recent advances in the modification of taste and food preferences following bariatric surgery

“…Lingual expression of the sweet taste receptor, T1R3, is lower in obesity-prone rats [97]. The detection of tastants by lingual taste receptors leads to the induction of signaling cascades which activate gustatory nerves to transmit sensory information to brain regions associated with the regulation of gustatory information, food intake and reward [107][108][109][110]. Obese animal models and human patients with T2D demonstrate alterations in fat and sucrose preferences and patients with T2D crave higher carbohydrate (sweet taste) foods, which is associated with poor glycemic control [81,94,103,111,112].…”

Neural responsivity during soft drink intake, anticipation, and advertisement exposure in habitually consuming youth

“…In contrast, obese versus lean individuals show less striatal activity during palatable food intake (12)(13)(14), which may delay meal termination if individuals are seeking the previously experienced pleasure from food intake. In support, objectively measured food intake beyond needs correlated positively with activity in attention and gustatory regions when anticipating palatable food receipt (15), and striatal response during intake correlated negatively with frequency of consumption of foods similar to those in the scan (16,17). Collectively, data demonstrate differences in neural responsivity to food stimuli during anticipation versus intake as a function of weight status and habitual intake, suggesting that regular consumption of energy-dense, palatable foods leads to hyper-responsivity of reward valuation regions to cues that signal potential intake and hypo-responsivity of reward regions during consumption.…”