Behavioral discrimination between sucrose and other natural sweeteners in mice: implications for the neural coding of T1R ligands

Abstract

In taste bud cells, two different T1R heteromeric taste receptors mediate signal transduction of sugars (the canonical "sweet" taste receptor, T1R2 + T1R3) and L-amino acids (the T1R1 + T1R3 receptor). The T1R1 + T1R3 receptor is thought to mediate what is considered the fifth basic taste quality "umami." However, a subset of L-amino acids is "sweet tasting" to humans and appears to possess a "sucrose-like" taste quality to nonhuman mammals. This suggests, to varying degrees, that all of these compounds activate a single neural channel that leads to the perception of sweetness. The experiments detailed here were designed to test the ability of mice to distinguish between sucrose and various others sugars and L-amino acids in operant taste discrimination tasks. Mice had at least some difficulty discriminating sucrose from L-serine, L-threonine, maltose, fructose, and glucose. For example, when concentration effects are taken into consideration, mice discriminated poorly, if at all, sucrose from glucose or fructose and, to a lesser extent maltose, suggesting that sugars generate a unitary perceptual quality. However, mice were able to reliably discriminate sucrose from L-serine and L-threonine. Data gathered using a conditioned taste aversion assay also suggest that, although qualitatively similar to the taste of sucrose, L-serine and L-threonine generate distinctive percepts. In conclusion, it appears that some signals from taste receptor proteins binding with sugars and some L-amino acids converge somewhere along the gustatory neuraxis. However, the results of these experiments also imply that sweet-tasting L-amino acids may possess qualitative taste characteristics that are distinguishable from the prototypical sweetener sucrose.

Figure 1.

Individual animal (symbols) and group mean ± SEM (gray bars) data for mice trained to discriminate sucrose from NaCl. Performance on all trials with a response is depicted collapsed across all stimuli during 1 week. *Statistically significant deviation from chance performance.

Figure 2.

Individual animal (symbols) and group mean ± SEM (gray bars) data are plotted across all test phases for mice initially trained to discriminate sucrose from NaCl. Black bars denote mean ± SEM performance during the last week of a stimulus control session (±SEM). Performance on all trials with a response is depicted collapsed across all stimuli during 1 week. *Statistically significant deviation from chance performance. Suc, Sucrose; Ser, l-serine; Glu, glucose; Mal, maltose; Fru, fructose; Thr, l-threonine.

Figure 3.

Mean ± SEM data for mice attempting to discriminate l-serine from sucrose. Performance, by concentration, on all trials with a response is depicted collapsed across 1 week. *Statistically significant deviation from chance performance.

Figure 4.

Mean ± SEM data for mice attempting to discriminate glucose from sucrose. Performance, by concentration, on all trials with a response is depicted collapsed across 1 week. *Statistically significant deviation from chance performance.

Figure 5.

Mean ± SEM data for mice attempting to discriminate maltose from sucrose. Performance, by concentration, on all trials with a response is depicted collapsed across 1 week. *Statistically significant deviation from chance performance.

Figure 6.

Mean ± SEM data for mice attempting to discriminate l-serine from sucrose for a second time. Performance, by concentration, on all trials with a response is depicted collapsed across 1 week. *Statistically significant deviation from chance performance.

Figure 7.

Mean ± SEM data for mice attempting to discriminate fructose from sucrose. Performance, by concentration, on all trials with a response is depicted collapsed across 1 week. *Statistically significant deviation from chance performance.

Figure 8.

Mean ± SEM data for mice attempting to discriminate l-threonine from sucrose. Performance, by concentration, on all trials with a response is depicted collapsed across 1 week. *Statistically significant deviation from chance performance.

Figure 9.

Mean ± SEM of the CS suppression ratio for each conditioned stimulus. A ratio of 1.0 signifies equal intake between the first and last conditioning trials, whereas a ratio less than or more than 1.0 signifies decreased or increased intake, respectively, in the last (fifth) conditioning trial relative to the first trial. *Significant difference from a ratio value of 1.0. #CS suppression ratio for each LiCl-injected group that was significantly lower than its corresponding control group.

Figure 10.

Mean ± SEM tastant/water lick ratios for the sucrose CS group for all test stimuli. The tastant/water lick ratio was calculated by dividing an animal's average licks to a given taste stimulus across trials by the average licks to water. The dashed line on the graph represents a tastant/water lick ratio of 1.0, which indicates licking to the taste stimulus was equivalent to licking to water. *Significant difference between the tastant/water lick ratios of the control and the conditioned groups.#Significant difference that survives the Bonferroni's α adjustment. C-L, 6.25 mm citric acid; C-H, 13.25 mm citric acid; N-L, 0.175 m NaCl; N-H, 0.375 m NaCl; Q-L, 0.325 mm QHCl; Q-H, 0.625 mm QHCl; S-L, 0.4 m l-serine; S-H, 1.0 m l-serine; Su-L, 0.2 m sucrose; Su-H, 0.6 m sucrose; T-L, 0.175 m l-threonine; T-H, 0.7 m l-threonine; CS, 0.4 m sucrose.

Figure 11.

Mean ± SEM tastant/water lick ratios for the l-serine CS group for all test stimuli. All details are the same as that described for Figure 10.

Figure 12.

Mean ± SEM tastant/water lick ratios for the l-threonine CS group for all test stimuli. All details are the same as that described for Figure 10.