Bitter Taste Stimuli Induce Differential Neural Codes in Mouse Brain

David M Wilson,Christian H Lemon,John D Boughter,Wolfgang Meyerhof

doi:10.1371/journal.pone.0041597

David M Wilson, Christian H Lemon + Show 2 more

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https://doi.org/10.1371/journal.pone.0041597

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Abstract

A growing literature suggests taste stimuli commonly classified as “bitter” induce heterogeneous neural and perceptual responses. Here, the central processing of bitter stimuli was studied in mice with genetically controlled bitter taste profiles. Using these mice removed genetic heterogeneity as a factor influencing gustatory neural codes for bitter stimuli. Electrophysiological activity (spikes) was recorded from single neurons in the nucleus tractus solitarius during oral delivery of taste solutions (26 total), including concentration series of the bitter tastants quinine, denatonium benzoate, cycloheximide, and sucrose octaacetate (SOA), presented to the whole mouth for 5 s. Seventy-nine neurons were sampled; in many cases multiple cells (2 to 5) were recorded from a mouse. Results showed bitter stimuli induced variable gustatory activity. For example, although some neurons responded robustly to quinine and cycloheximide, others displayed concentration-dependent activity (p<0.05) to quinine but not cycloheximide. Differential activity to bitter stimuli was observed across multiple neurons recorded from one animal in several mice. Across all cells, quinine and denatonium induced correlated spatial responses that differed (p<0.05) from those to cycloheximide and SOA. Modeling spatiotemporal neural ensemble activity revealed responses to quinine/denatonium and cycloheximide/SOA diverged during only an early, at least 1 s wide period of the taste response. Our findings highlight how temporal features of sensory processing contribute differences among bitter taste codes and build on data suggesting heterogeneity among “bitter” stimuli, data that challenge a strict monoguesia model for the bitter quality.

Highlights

We commonly describe our taste experience using sensory categories, including sweet, salty, sour, and bitter
Psychophysical data from humans [20,21,22] and rodents [23,24] show wide variation in sensitivity to diverse bitter stimuli and rats can discriminate between select bitter stimuli in taste detection paradigms [25], which would follow from differences in gustatory neural codes among bitters
This study found differences among central neural codes for individual bitter stimuli in two lines of mice and discovered that the early phase of the taste response carries these differences

Summary

Introduction

We commonly describe our taste experience using sensory categories, including sweet, salty, sour, and bitter. These categories, or qualities, have served diverse purposes in gustatory neurobiology research, from a convenience for stimulus classification to the basis for theories on the neural code for taste. Some evidence suggests that all T2R receptors are expressed by one type of taste receptor cell in taste buds of the oral cavity [3,5], predicting that all bitter stimuli should elicit a singular neural code. Molecular studies of mouse and human taste papillae have revealed heterogeneous expression of T2R receptors across taste bud cells (TBCs) [4,14]. Psychophysical data from humans [20,21,22] and rodents [23,24] show wide variation in sensitivity to diverse bitter stimuli and rats can discriminate between select bitter stimuli in taste detection paradigms [25], which would follow from differences in gustatory neural codes among bitters

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