Flavor Preferences in Animals: Role of Mouth and Gut Nutrient Sensors
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1
Brooklyn College of the City University of New York, Psychology, United States
Food appetite and preference are greatly influenced by taste, odor, and texture stimuli that are integrated in the brain as flavor sensations. One of the most potent flavor elements is the sweet taste of sugar. In mammals, sugar taste is detected primarily by two receptor proteins, T1R2 and T1R3, that join together to form a sweet taste receptor that responds to a variety of sugars and non-nutritive sweeteners [1]. The flavor of fat is also a source of food pleasure, which includes a taste component that influences the preference for fatty foods in some animals. The gustatory detection of fat is thought to involve lipid binding proteins including CD36, GPR120, and GPR40 located in taste receptor cells [1]. Another more subtle flavor component is umami, the taste of glutamate and certain nucleotides that adds a savory flavor to foods [1]. While many mammals have an innate preference for sweet and perhaps for fatty and umami tastes as well, most preferences for complex flavors are acquired in part through learned associations with the nutritional properties of foods. Social and cultural factors also contribute to learned flavor preferences, particularly in humans.
Food is “tasted” not only in the mouth but also in the gut where there are taste receptors and other nutrient sensors that detect sugar, fat, and protein [2]. There is extensive research on how nutrients in the gut generate neural and hormonal “satiation” signals that terminate meals and maintain post-meal satiety. Less well known is that nutrient actions in the gut can stimulate eating and condition flavor preferences though a process referred to as “appetition” [3]. Appetition has been most intensively studied in laboratory rodents. In a prototypical experiment, mice are offered flavored non-nutritive solutions (CS, conditioned stimuli) on alternate days with one flavor (CS+) paired with intragastric (IG) infusions of a sugar solution and a different flavor (CS-) paired with a water infusion. Flavor preference is then assessed in a two-bottle test with the CS+ vs. CS-. Numerous studies demonstrate that animals consume more of the sugar-paired CS+ flavor than of the water-paired CS- flavor during training and strongly prefer the CS+ to CS- in the choice test. Preferences are learned by hungry as well as freely fed animals and for initially unpalatable tastes (e.g., bitter) as well as palatable flavors (e.g., sweet cherry). Once learned, the CS+ preference persists for many days to weeks even in the absence of nutrient infusions.
The upper intestinal tract is a primary site where sugars act to condition flavor preferences, although the portal vein region near the liver is also implicated in sugar conditioning [2]. The discovery that the T1R2/T1R3 sweet receptor proteins are expressed in intestinal cells raised the possibility that the same receptors that trigger sugar appetite in the mouth also mediate postoral sugar appetition in the gut. However, several findings refute this attractive idea. In particular, sweet-tasting compounds differ substantially in their ability to condition flavor preferences when infused in the gut: IG glucose is much more effective than IG fructose in conditioning a CS+ preference whereas IG sucralose, a nonnutritive sweetener, conditioned a CS- preference [2]. In addition, sweet taste-impaired T1R3 knockout (KO) mice that are indifferent to sugars in the mouth develop normal preferences for a CS+ flavor paired with IG sucrose. These findings implicate glucose-specific intestinal sensors (SGLT1 and SGLT3) in sugar-conditioned preferences. This is supported by the flavor conditioning action in mice of the nonmetabolizable glucose analog α-methyl-D-glucopyranoside, which is an SGLT1/SGLT3 ligand [4]. The postoral appetition effects of sugar but not nonnutritive sweeteners explain why mice learn to prefer sucrose over isosweet sucralose solutions.
Like sugar, fat has postoral appetition effects. IG infusions of a soybean oil emulsion stimulate the intake of and preference for a CS+ flavor relative to a water-paired CS- flavor in food-restricted and freely-fed mice. Postoral fat conditioning is impaired in mice lacking GPR40 and GPR120 fatty acid receptors [5]. Although these receptors are implicated in fatty acid taste in the mouth, GPR40/120 KO mice displayed normal preferences for soybean oil in two-bottle oil vs. water tests [5]. So as in the case of sugar, different sensors are implicated in oral and post-oral fat-based flavor preferences.
Although less extensively studied, IG infusions of protein and glutamate solutions condition flavor preferences in rats and mice [2]. The postoral sensors mediating this form of flavor conditioning have not been identified but the T1R3 component of the umami receptor in the gut does not appear to be involved.
Little is known about the appetition signals generated by gut nutrient sensors. Sugar and fat appetition is not blocked by visceral nerve deafferentation, implying a gut-brain hormonal pathway, but this requires further research [2 and Figure 1]. In contrast, vagal nerve transection impairs flavor conditioning by IG glutamate infusions indicating the involvement of gut-brain neural signals. Gut nutrient signals do not evoke flavor sensations but rather operate on brain systems that enhance the reward evaluation of flavor sensations generated in the mouth by taste, odor, and trigeminal stimuli. As discussed elsewhere [6] and by Ivan De Araujo at this conference, these systems include ventral and dorsal dopamine reward circuits.
Acknowledgements
Supported by NIH grant DK031135
References
1. Chaudhari N, Roper SD. (2010) J Cell Biol 190:285-296.
2. Sclafani A, Ackroff K. (2012) Am J Physiol Regul Integr Comp Physiol 302:R1119-R1133.
3. Sclafani A. (2013) Appetite 71:454-458.
4. Zukerman S, Ackroff K, Sclafani A. (2013) Am J Physiol Regul Integr Comp Physiol 305:R840-R853.
5. Sclafani A, Zukerman S, Ackroff K. (2013) Am J Physiol Regul Integr Comp Physiol 305:R1490-R1497.
6. Sclafani A, Touzani K, Bodnar RJ (2011) Physiol & Behav 104:64-68.
Keywords:
Appetitition,
flavor preferences,
gut,
Lipid Binding Proteins,
Postoral Reward,
Taste Receptors
Conference:
Science of Human Flavor Perception, New York, United States, 9 May - 9 May, 2014.
Presentation Type:
Abstract
Topic:
Science of Human Flavor Perception
Citation:
Sclafani
A
(2015). Flavor Preferences in Animals: Role of Mouth and Gut Nutrient Sensors.
Front. Integr. Neurosci.
Conference Abstract:
Science of Human Flavor Perception.
doi: 10.3389/conf.fnint.2015.03.00004
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Received:
28 Jul 2014;
Published Online:
30 Jan 2015.
*
Correspondence:
Prof. Anthony Sclafani, Brooklyn College of the City University of New York, Psychology, Brooklyn, NY, United States, anthonys@brooklyn.cuny.edu