Narrowly and Broadly Tuned Peripheral Gustatory Neurons Cooperate to Encode Three Behaviorally Relevant Stimulus Categories.

Peripheral taste neurons vary in tuning breadth; some respond selectively to a single stimulus (narrowly tuned) and others respond to multiple stimuli (broadly tuned). How these differences contribute to taste coding remains unclear. We recorded calcium responses from 280 geniculate ganglion neurons to five or seven taste stimuli in male and female mice. Using five stimuli, 47% of neurons were narrowly tuned, while 53% responded to multiple stimuli. Hierarchical cluster analysis revealed five functional groups with five stimuli and six with seven stimuli, suggesting that the number of clusters is sensitive to the stimulus set rather than representing a fixed number of biologically distinct taste neuron "types". Principal component analysis (PCA) revealed three stimulus categories: (1) bitter, sour, and non-sodium salts (aversive), (2) sucrose and umami (caloric/appetitive), and (3) sodium salts (sodium-specific). Both narrowly tuned neurons and broadly tuned within a single category contributed to this categorization. In contrast, 40% of the neurons were broadly tuned across categories and did not cluster with specific stimulus types. These cross-category neurons were more likely to exhibit mixture sub-additivity-lower than additive responses-suggesting they could have a distinct role in encoding intensity or chemical context. Finally, we show Type II taste bud cells are required for representing these categories and mediating mixture sub-additivity between sweet and sour stimuli. These results suggest peripheral gustatory neurons primarily function to categorize taste stimuli into three groups. Furthermore, differing roles for narrowly tuned and broadly tuned neurons may be a key organizing principle of peripheral taste representation.Significance statement How the peripheral gustatory system encodes taste information remains unclear. We found that both narrowly tuned and broadly tuned peripheral taste neurons categorize seven taste stimuli into three groups: innately aversive, caloric/innately appetitive, and sodium-specific. These three categories are behaviorally relevant but do not represent single taste qualities. However, some broadly tuned neurons respond to stimuli across categories and have a sub-additive response to mixtures, suggesting a separate role for these neurons, perhaps representing stimulus context. Finally, mixture sub-additivity for some stimuli requires the convergence of sensory information from Type II and Type III cells. These findings are contrary to traditional models focusing solely on taste quality and instead support a focus on hedonics and contextual representations within peripheral taste neurons.