Narrowly and Broadly Tuned Peripheral Gustatory Neurons Cooperate to Encode Three Behaviorally Relevant Stimulus Categories
Description
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.
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These data are peak deltaF/F calcium responses average across two presentations of the same taste stimuli. Page 1 list stimulus concentrations. Each sheet represents a different combination of stimuli or a different group of animals. normalized relative responses are show to the right of the full response. Responses significantly above baseline are bold green. The geniculate ganglion was exposed using a dorsolateral approach. Once exposed, the preparation was transferred to our custom epifluorescence microscope and positioned under a 10×, 0.5 NA long-working-distance objective. The cell bodies of peripheral taste neurons in the geniculate ganglion were imaged for Ca2+ responses during automated stimulation of the tongue. Video recordings were performed during all trials using a scientific complementary metal–oxide–semiconductor video camera (pco.panda 4.2) at 2 fps. ROIs were selected in ImageJ using the magic wand tool. Custom MATLAB scripts (MathWorks), made publicly available (https://github.com/Dalston817/calciumImagingROITools), were used to calculate the relative change in fluorescence (ΔF/F0). The fluorescence signal of a C-shaped area surrounding each ROI was subtracted from the cell response to remove potential contributions of out-of-focus signals. Peripheral taste neurons were considered responsive to a given stimulus if ΔF/F0 was greater than five times the standard deviation of the 20 s baseline preceding the stimulus. The camera recorded all responses for the duration of the experiment.
Institutions
- University of Louisville