Food Reward in the Absence of Taste Receptor Signaling

Abstract

Food palatability and hedonic value play central roles in nutrient intake. However, postingestive effects can influence food preferences independently of palatability, although the neurobiological bases of such mechanisms remain poorly understood. Of central interest is whether the same brain reward circuitry that is responsive to palatable rewards also encodes metabolic value independently of taste signaling. Here we show that trpm5-/- mice, which lack the cellular machinery required for sweet taste transduction, can develop a robust preference for sucrose solutions based solely on caloric content. Sucrose intake induced dopamine release in the ventral striatum of these sweet-blind mice, a pattern usually associated with receipt of palatable rewards. Furthermore, single neurons in this same ventral striatal region showed increased sensitivity to caloric intake even in the absence of gustatory inputs. Our findings suggest that calorie-rich nutrients can directly influence brain reward circuits that control food intake independently of palatability or functional taste transduction.

The role of dopamine in the pursuit of nutritional value

“…Whereas wild-type mice show a strong preference for sucrose over water if given short access in a two bottle taste test, trpm5-/-mice show no preference [22]. In this study, given multiple two bottle training sessions with sipper position stable across session, mice did develop a preference for the sipper associated with sucrose.…”

“…One example is that knockout of the TRPM5 channel, which is essential for the transduction of sweet taste (and bitter and umami), has been used to generate mice that are 'sweet-blind'. This mutant line has allowed study of the post-ingestive effects of ingested sugars in isolation from taste-mediated effects [22].…”

“…In general, these substances are readily consumed by mice and rats and elicit appetitive orofacial reactions if infused intraorally, suggesting a positive hedonic evaluation [28,29]. Moreover, mice and rats show increased dopamine efflux and dopamine release in response to free consumption or intraoral delivery of nonnutritive sweeteners [22,30,31]. However, the extent to which these non-nutritive compounds participate in reinforcement/conditioning and how they interact with dopamine signalling during these processes is less clear.…”

“…Conditioned responses to other cues are also reduced or abolished to non-nutritive sweeteners. For example, mice fail to condition to bottle position associated with the non-nutritive sweetener, sucralose, whereas if sucrose is used in its place they do learn the association [22,35].…”

The Ala54Thr polymorphism in the fatty acid-binding protein 2 gene leads to higher food intake in Japanese women

“…The differences in glucoregulatory function and lipid oxidation might be partly explained by the genotype-dependent eating behavior. In addition, de Araujo et al 10 reported that sucrose intake induces dopamine release in the ventral striatum of Trpm5 knockout (sweet-blind) mice, indicating that calories and nutrients can directly influence brain reward circuits that control food intake independently of palatability or functional taste transduction.…”