Taste coding in the nucleus of the solitary tract of the awake, freely licking rat

Abstract

It is becoming increasingly clear that the brain processes sensory stimuli differently according to whether they are passively or actively acquired, and these differences can be seen early in the sensory pathway. In the nucleus of the solitary tract (NTS), the first relay in the central gustatory neuraxis, a rich variety of sensory inputs generated by active licking converge. Here, we show that taste responses in the NTS reflect these interactions. Experiments consisted of recordings of taste-related activity in the NTS of awake rats as they freely licked exemplars of the five basic taste qualities (sweet, sour, salty, bitter, umami). Nearly all taste-responsive cells were broadly tuned across taste qualities. A subset responded to taste with long latencies (>1.0 s), suggesting the activation of extraoral chemoreceptors. Analyses of the temporal characteristics of taste responses showed that spike timing conveyed significantly more information than spike count alone in almost one-half of NTS cells, as in anesthetized rats, but with less information per cell. In addition to taste-responsive cells, the NTS contains cells that synchronize with licks. Since the lick pattern per se can convey information, these cells may collaborate with taste-responsive cells to identify taste quality. Other cells become silent during licking. These latter "antilick" cells show a surge in firing rate predicting the beginning and signaling the end of a lick bout. Collectively, the data reveal a complex array of cell types in the NTS, only a portion of which include taste-responsive cells, which work together to acquire sensory information.

Figure 1.

Diagram of the stimulus delivery paradigm. Taste stimuli are presented for five consecutive licks followed by five water rinse licks delivered on a VR5 schedule. Each lick is symbolized by a vertical line: licks that result in taste stimulus delivery are red and green; water rinse licks are blue; dry licks are in gray.

Figure 2.

Taste response characteristics in the NTS of awake, freely licking rats. A, The distribution of cells that respond to different numbers of taste qualities in cells tested with the low concentration of sucrose (top; n = 25 cells in 7 rats) and those tested with the high concentration of sucrose (bottom; n = 31 cells in 18 rats). Percentage of the total number of neurons in each category are indicated on the graph. B, The distribution of the various types of responses that were recorded for each taste stimulus (n = 56 cells).

Figure 3.

Mean response magnitudes in spikes per second ± SEM across taste-responsive cells in the NTS in awake, freely licking rats. Baseline firing rates are subtracted from taste-evoked firing rates. A, Excitatory responses (n = 198 total). B, Inhibitory responses (n = 140 total).

Figure 4.

Example of a broadly tuned taste-responsive NTS cell. The top of each panel shows a raster of taste-evoked spike activity; each dot indicates the occurrence of a spike; each colored dot indicates the delivery of a fluid with a lick; the light blue dots indicate the delivery of water with a lick. Dry licks that occur between water deliveries following stimulus trials are not shown. The bottom of each panel shows PSTHs of taste responses. Time bin, 100 ms. The inset at the top right shows the waveform of the cell.

Figure 5.

Cumulative distribution of latencies of excitatory (filled symbols) and inhibitory (open symbols) taste responses for all taste stimuli plus water, as a fraction of the total. The numbers of excitatory responses are as follows: low sucrose, 9; high sucrose, 19; NaCl, 36; citric acid, 47; quinine, 34; MSG, 21; water, 32. The numbers of inhibitory responses are as follows: low sucrose, 13; high sucrose, 10; NaCl, 24; citric acid, 22; quinine, 28; MSG, 22; water, 21.

Figure 6.

A, Example of taste responses in an NTS cell with a long-latency response to NaCl and quinine. There were 24 cells that showed such responses. B, Example of taste responses in an NTS cell with short-latency excitatory responses to NaCl and MSG, and a long-latency inhibitory response to quinine. There were 14 cells recorded from 12 rats that showed both short- and long-latency responses. Rasters and PSTHs are as in Figure 4. The insets at top left show the waveform of the cell.

Figure 7.

Taste-evoked responses in an NTS cell that showed prominent lick-related activity. There were 14 such cells. Rasters and PSTHs are as in Figure 4. The inset at bottom right shows the waveform of the cell. A, Responses are shown to all taste stimuli plus water for 5 s after the initial stimulus lick. B, Responses to all stimulus licks are shown at an expanded timescale (time bin, 10 ms) to illustrate lick-related activity. Note that this is selective for specific stimuli: it is prominent for NaCl, but for citric acid, it is no larger than the response to a dry lick (final panel).

Figure 8.

Taste-evoked activity in an NTS cell that incrementally increased with successive stimulus licks. Rasters and PSTHs are as in Figure 4. A, Responses to all tastes and water. B, Responses to the first and fifth licks in the five lick stimulus delivery sequence showing that the fifth lick produces a response but the first lick does not. Time bin, 10 ms. The inset at the right shows the waveform of the cell.

Figure 9.

Summary of results of metric space analyses of taste responses in NTS cells for response intervals following the first stimulus lick of the five lick sequence. Response intervals of 100 ms, 200 ms, 500 ms, 1.0 s, 1.5 s, and 2.0 s of activity were analyzed. Values plotted for H_count and H_max are the average amount of information per cell (in bits), across the population of 40 taste-responsive cells in which at least six presentations of each stimulus were recorded. H_count considers information carried by spike count and H_max takes into account the temporal pattern of the response as well. The number next to each point is the number of cells for which the information estimate was significantly greater than 0. The trace labeled “lick” is the corresponding estimate of information (H_max) contained in the temporal pattern of the lick activity. Inset, Geometric mean of q_max for all cells in which the information estimate is significantly greater than 0, and for which temporal coding was present (H_max > H_count).

Figure 10.

Information (in bits) about taste quality conveyed by spike count (H_count) versus the maximum information (H_max). Distance above the dashed diagonal line corresponds to the amount of additional information conveyed by the temporal aspects of the response; for a point on the diagonal line (H_max = H_count), all information is carried by spike count. The symbol indicates whether the temporal component of the information is accounted for by the firing rate envelope (gray squares, H_max < H_exchange + 2SD; n = 11), or, alternatively, whether there is an additional contribution from individual spike times (black circles, H_max > H_exchange + 2SD; n = 7).

Figure 11.

Information conveyed by taste-responsive cells during the 120 ms following individual stimulus licks. Only cells for which the amount of information is significantly greater than 0 are shown. If temporal aspects of the response convey information, the amount of information is color coded according to the key at top right; the cells for which this information is carried entirely by spike count (q_max = 0) are shown as blue. It can be seen that individual cells convey information about taste quality at different times during the five licks of stimulus presentation.

Figure 12.

Examples of NTS cells with strong lick-related activity (n = 37). Rasters and PSTHs are as in Figure 4. Insets, PSTH triggered by dry licks (top) and the spike waveform (bottom). A, A taste-responsive cell (left) with activity that was also time-locked to the dry licks (right). There were 14 cells that showed both taste and lick-related activity. B, A cell with no response to taste stimuli, but which showed strong lick-related activity. There were 23 cells that showed lick-related activity but did not respond to taste stimuli. For both A and B, note the difference in time scales of the taste responses and dry lick PSTH plots: left, time bin, 100 ms; right, time bin, 10 ms.

Figure 13.

Firing pattern of an antilick cell (n = 28). A, Cellular activity, shown in yellow, along with licks, shown as vertical red lines. Top, Cell fires almost exclusively when the rat is not licking. Bottom, Activity at an expanded timescale is shown, illustrating the surge in firing rate before and after a lick bout. The top right inset shows the waveforms of the cell. B, PSTH of the firing pattern of the cell at the transitions from an interbout interval to a lick bout and vice versa. (A lick bout was defined as a period of at least 1 s of continuous licking; an interbout interval was defined as a period of at least 1 s where there were no licks.) Time bin, 100 ms. See text for details. C, Rasters corresponding to B.

Figure 14.

Coronal sections through the NTS showing locations of lesions marking recording sites. Lesions in 17 rats were reconstructed. The numbers in the top left of each panel indicate millimeters posterior to bregma. Scale bar, 1 mm. Abbreviations are as follows: NTS, nucleus of the solitary tract; XII, nucleus of the hypoglossal nerve; MVe, medial vestibular nucleus.