Receptive fields of sensory neurons in the brain are usually restricted to a portion of the entire stimulus domain. At all levels of the gustatory neuraxis, however, there are many cells that are broadly tuned, i.e., they respond well to each of the basic taste qualities (sweet, sour, salty, and bitter). Although it might seem that this broad tuning precludes a major role for these cells in representing taste space, here we show the opposite-namely, that the tastant-specific temporal aspects (firing rate envelope and spike timing) of their responses enable each cell to represent the entire stimulus domain. Specifically, we recorded the response patterns of cells in the nucleus of the solitary tract (NTS) to representatives of four basic taste qualities and their binary mixtures. We analyzed the temporal aspects of these responses, and used their similarities and differences to construct the taste space represented by each neuron. We found that for the more broadly tuned neurons in the NTS, the taste space is a systematic representation of the entire taste domain. That is, the taste space of these broadly tuned neurons is three dimensional, with basic taste qualities widely separated and binary mixtures placed close to their components. Further, the way that taste quality is represented by the firing rate envelope is consistent across the population of cells. Thus, the temporal characteristics of responses in the population of NTS neurons, especially those that are more broadly tuned, produce a comprehensive and logical representation of the taste world.

In the nucleus of the solitary tract (NTS), electrophysiological responses to taste stimuli representing four basic taste qualities (sweet, sour, salty, or bitter) can often be discriminated by spike count, although in units for which the number of spikes is variable across identical stimulus presentations, spike timing (i.e., temporal coding) can also support reliable discrimination. The present study examined the contribution of spike count and spike timing to the discrimination of stimuli that evoke the same taste quality but are of different chemical composition. Responses to between 3 and 21 repeated presentations of two pairs of quality-matched tastants were recorded from 38 single cells in the NTS of urethane-anesthetized rats. Temporal coding was assessed in 24 cells, most of which were tested with salty and sour tastants, using an information-theoretic approach. Within a given cell, responses to tastants of similar quality were generally closer in magnitude than responses to dissimilar tastants; however, tastants of similar quality often reversed their order of effectiveness across replicate sets of trials. Typically, discrimination between tastants of dissimilar qualities could be made by spike count. Responses to tastants of similar quality typically evoked more similar response magnitudes but were more frequently, and to a proportionally greater degree, distinguishable based on temporal information. Results showed that nearly every taste-responsive NTS cell has the capacity to generate temporal features in evoked spike trains that can be used to distinguish between stimuli of different qualities and chemical compositions.

. Sensory neurons are generally tuned to a subset of stimulus qualities within their sensory domain and manifest this tuning by the relative size of their responses to stimuli of equal intensity. However, response size alone cannot unambiguously signal stimulus quality, since response size also depends on stimulus intensity. Thus a common problem faced by sensory systems is that response size (e.g., spike count) confounds stimulus quality and intensity. Here, using the gustatory system as a model, we asked whether temporal firing characteristics could disambiguate these axes. To address this question, we recorded taste responses of single neurons in the nucleus of the solitary tract (NTS, the first central gustatory relay) in anesthetized rats to a range of concentrations of NaCl and HCl and their binary mixtures. To assess the contribution of the temporal characteristics of the response to discrimination among tastants, a family of metrics that quantifies the similarity of two spike trains in terms of spike count and spike timing was used. Results showed that the spike count produced by different taste qualities and different concentrations overlapped in most cells, implying that information conveyed by spike count is imprecise. Multidimensional scaling analysis of taste responses using similarity of temporal characteristics showed that different taste qualities, intensities, and mixtures formed distinct clusters in this "temporal coding" taste space and were arranged in a logical order. Thus the temporal structure of taste responses in single cells in the NTS can simultaneously convey information about both taste quality and intensity. I N T R O D U C T I O NIn all sensory systems, individual cells are tuned to respond selectively to a certain set of stimuli. The variety of tuning curves across cells spans and defines the broader stimulus domain and enables the identification and discrimination of different stimuli. However, changes in stimulus intensity generally broaden those tuning curves and may produce confusion between a change in stimulus intensity and a change in identity. When the tuning (specificity) is narrow, the identity of the neuron can signal the identity of the stimulus (e.g., pitch, color, taste quality, etc.) and the relative firing rate can indicate intensity (e.g., loudness, brightness, concentration). In a system such as gustation, where most cells respond well to more than one taste quality (sweet, sour, salty, bitter, and perhaps umami), stimuli of different taste qualities can evoke equivalent firing rates if the concentrations are just right. As a result, in most cases firing rate alone cannot convey an unambiguous message about taste quality, especially in broadly tuned neurons.In many studies of taste-responsive cells in the CNS, groups of cells are defined by the stimulus that evokes the "best" or most robust response when exemplars of each basic taste quality are presented at moderate concentrations. Even though most cells are multisensitive across taste qualities, several researc...

The contribution of gustation to the perception of food requires an understanding of how neurons represent mixtures of taste qualities. In the periphery, separate groups of fibers, labeled by the stimulus that evokes the best (largest) response, appear to respond to each component of a mixture. In the brain, identification of analogous groups of neurons is hampered by trial-to-trial variability in response magnitude. In addition, convergence of different fiber types onto central neurons may complicate the classification scheme. To investigate these issues, electrophysiological responses to four tastants: sucrose, NaCl, HCl, and quinine, and their binary mixtures were recorded from 56 cells in the nucleus of the solitary tract (NTS, the 1st synapse in the central gustatory pathway) of the anesthetized rat. For 36 of these cells, all 10 stimuli were repeated at least five times (range: 5-23; median = 10). Results showed that 39% of these cells changed their best stimulus across stimulus repetitions, suggesting that response magnitude (firing rate) on any given trial produces an ambiguous message. Averaged across replicate trials, mixture responses most often approximated the response to the more effective component of the mixture. Cells that responded best to a taste mixture rather than any single-component tastant were identified. These cells were more broadly tuned than were cells that responded best to single-component stimuli and showed evidence of convergence from more than one best stimulus fiber type. Functionally, mixture-best cells may amplify the neural signal produced by unique configurations of basic taste qualities.