Variation in the gene Tas1r3 reveals complex temporal properties of mouse brainstem taste responses to sweeteners

Abstract

The gene Tas1r3 codes for the protein T1R3, which dimerizes with T1R2 to form a sweetener-binding receptor in taste cells. Tas1r3 influences sweetener preferences in mice, as shown by work with a 129.B6-Tas1r3 segregating congenic strain on a 129P3/J (129) genetic background; members of this strain vary in whether they do or do not have one copy of a donor fragment with the C57BL/6ByJ (B6) allele for Tas1r3 (B6/129 and 129/129 mice, respectively). Taste-evoked neural responses were measured in the nucleus of the solitary tract (NST), the first central gustatory relay, in B6/129 and 129/129 littermates, to examine how the activity dependent on the T1R2/T1R3 receptor is distributed across neurons and over time. Responses to sucrose were larger in B6/129 than in 129/129 mice, but only during a later, tonic response portion (>600 ms) sent to different cells than the earlier, phasic response. Similar results were found for artificial sweeteners, whose responses were best considered as complex spatiotemporal patterns. There were also group differences in burst firing of NST cells, with a significant positive correlation between bursting prevalence and sucrose response size in only the 129/129 group. The results indicate that sweetener transduction initially occurs through T1R3-independent mechanisms, after which the T1R2/T1R3 receptor initiates a separate, spatially distinct response, with the later period dominating sweet taste perceptions and driving sugar preferences. Furthermore, the current data suggest that burst firing is distributed across NST neurons nonrandomly and in a manner that may amplify weak incoming gustatory signals.