Rats Fail to Discriminate Quinine from Denatonium: Implications for the Neural Coding of Bitter-Tasting Compounds

Abstract

Recent molecular findings indicate that many different G-protein-coupled taste receptors that bind with "bitter-tasting" ligands are coexpressed in single taste receptor cells in taste buds, leading to the prediction that mammals can respond behaviorally to structurally diverse "bitter" tastants but cannot discriminate among them. However, recent in situ calcium-imaging findings imply that rat taste receptor cells are more narrowly tuned to respond to bitter-tasting compounds than had been predicted from molecular findings, suggesting that these animals can discriminate among these chemicals. Using an operant conditioning paradigm, we demonstrated that rats cannot discriminate between two structurally dissimilar bitter compounds, quinine hydrochloride and denatonium benzoate, despite the fact that these tastants are thought to stimulate different taste receptor cells. These rats were nonetheless able to show concentration-dependent avoidance responses to both compounds in brief-access tests and to discriminate among other taste stimuli, including quinine versus KCl, denatonium versus KCl, and NaCl versus KCl. Importantly, the concentrations were varied in the discrimination tests to render intensity an irrelevant cue. We conclude that denatonium and quinine produce a unitary taste sensation, leaving open the likely possibility that other compounds fall into this class. Although a broader array of compounds needs to be tested, our findings lend support to the hypothesis that there is only one qualitative type of bitterness. These results also highlight the need to confirm predictions about the downstream properties of the gustatory system, or any sensory system, based on upstream molecular and biophysical events.

Behavioral Discrimination between Sucrose and Other Natural Sweeteners in Mice: Implications for the Neural Coding of T1R Ligands

“…Monogeusia has been demonstrated in humans with some natural sweeteners (Breslin et al, 1996) and in rats with some "bitter" tastants (Spector and Kopka, 2002). To our knowledge, monogeusia for natural sweeteners had never been explicitly tested in a rodent model until the present study.…”

Limited taste discrimination in Drosophila

“…In mammals, quality-and intensity-based discrimination has been described (29,30), but experiments in which taste compounds were compared over a concentration range generally argue against intramodality discrimination (31)(32)(33). Why would taste systems evolve that allow animals to detect many compounds but maintain a limited ability to discriminate among them?…”

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

“…Throughout this report we have referred to DB as a bitter stimulus, simply because it is a selective agonist for a receptor belonging to the bitter T2R family, which has also been localized in the postoral GI tract, that evokes a similar sensation to other bitter tastants (e.g., quinine) upon contact with lingual receptors (7,43,50). However, it is unclear whether the DB stimulus that the rats are detecting in the intestine is encoded as bitter.…”