Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal “bitter taste” cue

Abstract

Schier LA, Davidson TL, Powley TL. Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal "bitter taste" cue. Am J Physiol Regul Integr Comp Physiol 301: R1557-R1568, 2011. First published August 24, 2011 doi:10.1152/ajpregu.00344.2011.-The discovery that cells in the gastrointestinal (GI) tract express the same molecular receptors and intracellular signaling components known to be involved in taste has generated great interest in potential functions of such post-oral "taste" receptors in the control of food intake. To determine whether taste cues in the GI tract are detected and can directly influence behavior, the present study used a microbehavioral analysis of intake, in which rats drank from lickometers that were programmed to simultaneously deliver a brief yoked infusion of a taste stimulus to the intestines. Specifically, in daily 30-min sessions, thirsty rats with indwelling intraduodenal catheters were trained to drink hypotonic (0.12 M) sodium chloride (NaCl) and simultaneously self-infuse a 0.12 M NaCl solution. Once trained, in a subsequent series of intestinal taste probe trials, rats reduced licking during a 6-min infusion period, when a bitter stimulus denatonium benzoate (DB; 10 mM) was added to the NaCl vehicle for infusion, apparently conditioning a mild taste aversion. Presentation of the DB in isomolar lithium chloride (LiCl) for intestinal infusions accelerated the development of the response across trials and strengthened the temporal resolution of the early licking suppression in response to the arrival of the DB in the intestine. In an experiment to evaluate whether CCK is involved as a paracrine signal in transducing the intestinal taste of DB, the CCK-1R antagonist devazepide partially blocked the response to intestinal DB. In contrast to their ability to detect and avoid the bitter taste in the intestine, rats did not modify their licking to saccharin intraduodenal probe infusions. The intestinal taste aversion paradigm developed here provides a sensitive and effective protocol for evaluating which tastants-and concentrations of tastants-in the lumen of the gut can control ingestion. chemoreceptor; gastrointestinal; denatonium benzoate; food learning; cholecystokinin CHEMORECEPTORS ARE INDISPENSABLE to the control of food intake. As taste receptors on the tongue and in the oral cavity, they supply signals critical for accepting and rejecting foods for consumption, promoting intake of palatable foods, and preparing the digestive system for the arrival of nutrients. Complementary to this early oral sensory processing, chemoreceptors in the stomach and intestines transduce signals from the lumen to adjust motility, secrete digestive enzymes, and initiate satiation (cf., 24). Accordingly, the gastrointestinal (GI) tract has been conventionally considered to have a more or less continuous sensory surface for tracking meals to engage and revise apposite and coordinated responses particular to the properties of the food and the body's physiological state. Despite th...

Rapid stimulus-bound suppression of intake in response to an intraduodenal nonnutritive sweetener after training with nutritive sugars predicting malaise

“…However, in the event that sweet-tasting ID Sucralose is too weak on its own or responding extinguishes with repeated exposure, direct pairing with LiCl, a noncaloric, noncarbohydrate, but still biologically relevant stimulus, might maintain responding and augment detection over repeated trials. In our previous study (37), rats did not learn to use a different nonnutritive sweetener, 9.75 mM Na Saccharin, to predict LiCl, in this same paradigm; thus, here we used an artificial sweetener that more effectively stimulates cytosolic Ca 2ϩ in oral sweet taste receptor cells and is a stronger stimulus for GLUT-2 upregulation in the intestine (25,27). To complement this, the second aim of the present studies was to evaluate whether rats can use the early intestinal sensory properties of a functional carbohydrate, and arguably more conventional intestinal stimulus (sucrose), to predict malaise and then to discern whether the sweet taste feature of that cue was encoded.…”

“…Each rat was fitted with an intraduodenal catheter according to procedures described in more detail elsewhere (37). Briefly, after an overnight fast, each rat was anesthetized (Nembutal, 60 mg/kg ip) and laparotomized.…”

“…5,13,20,32,41). To address such questions, we recently developed and employed a new behavioral paradigm to demonstrate that a bitter tastant in the duodenum produces stimulus-bound reductions in ongoing ingestion (37). The present set of experiments addresses similar functional questions using the same behavioral paradigm to evaluate the effects of sweet tastants in the duodenum.…”

“…In Schier et al (37), we developed a behavioral paradigm with the capacity to examine the detection and discrimination of early preabsorptive taste-like signals arising from the intestine and their effects on ongoing ingestive behavior, separate from any delayed postabsorptive or rewarding effects of the same stimuli. In this approach, a modified conditioned taste aversion, thirsty rats lick at sipper spouts for hypotonic NaCl for 30 min each day and receive brief (first 6 min) yoked intraduodenal (ID) infusions of either the same NaCl solution or an isomolar lithium chloride (LiCl) solution.…”

“…1, when a bitter taste cue denatonium benzoate (DB, 10 mM) was selectively added to the LiCl infusate to condition an intestinal taste aversion, rats readily learned to rapidly, but transiently, inhibit ongoing intake upon the arrival of the bitter stimulus to the intestine (Ref. 37, experiments 1 and 2).…”