The authors tested the hypothesis that obese individuals experience greater reward from food consumption (consummatory food reward) and anticipated consumption (anticipatory food reward) than lean individuals using functional magnetic resonance imaging (fMRI) with 33 adolescent girls (mean age = 15.7, SD = 0.9). Obese relative to lean adolescent girls showed greater activation bilaterally in the gustatory cortex (anterior and mid insula, frontal operculum) and in somatosensory regions (parietal operculum and Rolandic operculum) in response to anticipated intake of chocolate milkshake (vs. a tasteless solution) and to actual consumption of milkshake (vs. a tasteless solution); these brain regions encode the sensory and hedonic aspects of food. However, obese relative to lean adolescent girls also showed decreased activation in the caudate nucleus in response to consumption of milkshake versus a tasteless solution, potentially because they have reduced dopamine receptor availability. Results suggest that individuals who show greater activation in the gustatory cortex and somatosensory regions in response to anticipation and consumption of food, but who show weaker activation in the striatum during food intake, may be at risk for overeating and consequent weight gain.

The conscious perception of the hedonic sensory properties of caloric foods is commonly believed to guide our dietary choices. Current and traditional models implicate the consciously perceived hedonic qualities of food as driving overeating, whereas subliminal signals arising from the gut would curb our uncontrolled desire for calories. Here we review recent animal and human studies that support a markedly different model for food reward. These findings reveal in particular the existence of subcortical body-to-brain neural pathways linking gastrointestinal nutrient sensors to the brain's reward regions. Unexpectedly, consciously perceptible hedonic qualities appear to play a less relevant, and mostly transient, role in food reinforcement. In this model, gut-brain reward pathways bypass cranial taste and aroma sensory receptors and the cortical networks that give rise to flavor perception. They instead reinforce behaviors independently of the cognitive processes that support overt insights into the nature of our dietary decisions.

Processed foods compromise the fidelity of gut-brain signaling of food reinforcement

In rodents, food-predictive cues elicit eating in the absence of hunger (Weingarten, 1983). This behavior is disrupted by the disconnection of amygdala pathways to the lateral hypothalamus (Petrovich et al., 2002). Whether this circuit contributes to long-term weight gain is unknown. Using fMRI in 32 healthy individuals, we demonstrate here that the amygdala response to the taste of a milkshake when sated but not hungry positively predicts weight change. This effect is independent of sex, initial BMI, and total circulating ghrelin levels, but it is only present in individuals who do not carry a copy of the A1 allele of the Taq1A polymorphism. In contrast, A1 allele carriers, who have decreased D2 receptor density (Blum et al., 1996), show a positive association between caudate response and weight change. Regardless of genotype, however, dynamic causal modeling supports unidirectional gustatory input from basolateral amygdala (BLA) to hypothalamus in sated subjects. This finding suggests that, as in rodents, external cues gain access to the homeostatic control circuits of the human hypothalamus via the amygdala. In contrast, during hunger, gustatory inputs enter the hypothalamus and drive bidirectional connectivity with the amygdala. These findings implicate the BLA–hypothalamic circuit in long-term weight change related to nonhomeostatic eating and provide compelling evidence that distinct brain mechanisms confer susceptibility to weight gain depending upon individual differences in dopamine signaling.