Variability in responses and temporal coding of tastants of similar quality in the nucleus of the solitary tract of the rat

Abstract

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.

Figure 1

Mean ± SEM of all responses to each tastants tested. Abbreviations: S, sucrose; F, fructose; N, NaCl; L, LiCl; H, HCl; C, citric acid; Q, quinine; U, urea.

Figure 2

Response rate (sps) across trials for salty and sour tastants in two cells. Abbreviations are as follows: N, NaCl; L, LiCl; H, HCl; C, citric acid. Top graph shows a cell with responses to different qualities (salty and sour) that reverse their order of effectiveness on different blocks of trials. Bottom shows a cell with responses to the same taste quality (salty) that reverse their order of effectiveness on different blocks of trials.

Figure 3

Graph of the mean ± SEM coefficient of variation (CV, standard deviation divided by the mean) across cells for each stimulus. Only those cells that showed at least three significant responses were included. Abbreviations and numbers of cells included were as follows: S, sucrose, n = 5; F, fructose, n = 5; N, NaCl, n = 35; L, LiCl, n = 33; H, HCl, n = 25; C, citric acid, n = 21; Q, quinine, n = 8; U, urea, n = 5.

Figure 4

A. Peristimulus-time histograms (PSTHs) of responses to NaCl, LiCl and HCl. B. Responses (sps) to NaCl (N), LiCl (L), HCl (H) and citric acid (C) across trials. C. Metric space analysis of information contributed by responses (filled squares) at various levels of temporal precision, q(1/sec). Results of exchange (open squares) control analysis are also shown. Left graph shows that spike timing contributes a significant amount of information to the discrimination of NaCl vs. LiCl at q = 32, as indicated by a star. Right graph shows that spike count provides perfect discrimination of NaCl vs. HCl, as indicated by H = 1.0 at q = 0. See text for details.

Figure 5

Example of a cell for which the rate envelope primarily accounts for the distinction between responses to HCl and citric acid. A. PSTHs of responses to HCl and citric acid. B. Responses (sps) to NaCl (N), LiCl (L), HCl (H) and citric acid (C) across trials. C. Metric space analysis of information contributed by spike timing of the responses (filled squares) at various levels of temporal precision, q(1/sec). Results of exchange (open circles) and resampling (open diamonds) control analyses are also shown. Spike timing provides no more information than the exchange analyses. See text for details.

Figure 6

Information conveyed by H_count relative to the contribution of the temporal characteristics of a response to the total amount of information conveyed by taste responses. A. Graph of H_count plotted against H_max – H_count for all stimulus-stimulus comparisons for all NTS cells that were analyzed for temporal coding (n = 25). Filled circles indicate comparisons of tastants of similar quality and open circles indicate comparisons of tastants of dissimilar quality. B. Histogram of the percent of the total number of stimulus-stimulus comparisons that showed various ratios of the contribution of temporal coding (H_max –H_count) in relation to the contribution of spike count (H_count). Solid bars indicate comparisons of tastants of similar quality and hashed bars indicate comparisons of tastants of dissimilar quality. See text for details.

Figure 7

Incidence of temporal coding by spike timing (blue squares), rate envelope (yellow squares) and spike count (pink squares). Empty squares indicate that the total information contributed by the response was low; i.e. H_max < 0.1. Numbers indicate the value of q at H_max for cells that show a significant contribution of spike timing. Upper set of rows: cells tested with pairs of salty and sour stimuli. Lower set of rows: cells tested with pairs of salty and bitter stimuli.