Do gastrointestinal taste receptors contribute to associative learning and foraging behavior?1

Abstract

Foraging behavior is an expression of learning, context, and experience arising from integration of sensory information obtained during feeding with postingestive consequences of food ingestion. Although it has been well established that gustatory and olfactory systems of the mouth and nose provide sensory information to the consumer (in the form of flavor), sweet and bitter taste receptors have recently been identified in the intestinal tract of humans and rodents. It remains possible that sensory information generated in the gut could contribute to the learning process. Thus, a series of experiments was conducted to determine if classical associative learning occurs when the conditional stimulus circumvents oronasal presentation via direct delivery to the gut or peritoneal cavity. Mice receiving an intragastric infusion of 5 mM sodium saccharin immediately followed by LiCl administration demonstrated a significant decrease in preference for 5 mM saccharin in 4 consecutive 23 h, 2-bottle preference tests versus water (P = 0.0053). Saccharin was highly preferred in mice receiving intragastric (IG) saccharin only or interperitoneal (i.p.) injection of LiCl only. This reduced preference indicated that mice "tasted" saccharin infused into the gut. However, efforts to replicate with a reduced infusion volume failed to result in decreased preference. To understand if there were alternative pathways for oral detection of infused saccharin, mice received intragastric infusions (5.4 mM) and i.p. injections (10.8 mM) of sodium fluorescein. Fluorescence was observed from the tongues and esophagi of mice infused with volumes of 0.5 mL or more or injected with volumes of 0.25 mL or greater. Interperitoneal injections of 5 mM saccharin in mice resulted in reduced preference for 5 mM saccharin presented orally in 2-bottle preference tests (P = 0.0287). Oral delivery of a 500-fold less concentration of saccharin (0.01 mM) during conditioning resulted in a similar preference expression as shown in the initial IG experiment. These results demonstrate that although compounds may be tasted in the mouth absent of oral contact, associative learning is attenuated. Therefore, intestinal taste receptors are unlikely to participate directly in learning and recognition of foods during foraging events.