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 in response to five or seven taste stimuli. 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 cluster number depends on the stimulus set rather than intrinsic neuron types. However, principal component analysis (PCA) revealed three consistent 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 those broadly tuned within a single category contributed to this categorization. In contrast, 40% of neurons were broadly tuned across categories and did not cluster with specific stimulus types. These cross-category neurons were more likely to exhibit mixture suppression—lower than additive responses to stimulus combinations—suggesting they could have a distinct role in encoding intensity or chemical context. Lastly, we show Type II taste bud cells are required for representing these categories and mediating mixture suppression between sweet and sour stimuli. These results suggest peripheral gustatory neurons primarily function to categorize stimuli based on into three groups, rather than five basic taste qualities. Furthermore, differing roles for narrowly tuned and broadly tuned neurons may be a key organizing principle of peripheral taste coding.