Neural coding of taste by simultaneously recorded cells in the nucleus of the solitary tract of the rat

Abstract

The nucleus of the solitary tract (NTS) receives input from taste buds on the rostral tongue from the chorda tympani (CT) nerve. How this input is processed by the NTS was the subject of the present investigation. Here we used tetrodes to record from pairs or small groups of NTS cells as they responded to taste stimuli or electrical stimulation of the CT nerve in urethane-anesthetized rats. Once a pair (or small group) of NTS cells were isolated and identified as showing an evoked response to CT nerve stimulation, taste stimuli were presented in separate trials. Tastants consisted of 0.1 M NaCl, 0.01 M HCl, 0.01 M quinine HCl, and 0.5 M sucrose. Responses to various patterns of CT stimulation were then recorded. Functional connections among simultaneously recorded NTS cells were implied from analysis of cross-correlation functions of spike trains. We identified four groups of cells, not all of which responded to taste, with staggered latencies of response to CT nerve stimulation, ranging from ∼3 to 35 ms in ∼8- to 12-ms increments. Analyses of putative functional connectivity along with latencies of CT-evoked responses suggested that CT input arrives at the NTS in pulses or waves, each of which activates recurrent excitatory connections among NTS cells. These actions may amplify the incoming signal and refine its temporal pattern.

Fig. 1.

A: frequency distribution of the latency of evoked response to electrical stimulation of the chorda tympani (CT) nerve across 102 nucleus of the solitary tract (NTS) cells. Black bars indicate taste-responsive cells; gray bars indicate non-taste-responsive cells. Values along the x-axis indicate the upper limit of each bin. Arrows above the graph indicate latency groups. B: dendrogram showing results of a hierarchical cluster analysis conducted on latency and jitter for each cell. See text for details.

Fig. 2.

Latency and jitter among NTS cells in response to CT nerve stimulation. A: neural firing of cells in each latency group in response to electrical pulses delivered to the CT nerve. B: mean + SE latencies of CT-evoked responses in each latency group. C: peristimulus time histograms of variability of the latency of response to CT nerve stimulation in each latency group. D: mean + SE jitter (SD) (ms) in each latency group.

Fig. 3.

Responses to the 4 prototypical taste stimuli across cells in each latency group. Cells are aligned vertically in descending order of magnitude of their response to NaCl.

Fig. 4.

Functional connectivity among NTS cells. Latency (ms) refers to the evoked response to electrical stimulation of the CT nerve. Taste response magnitudes to the basic taste qualities are also shown. S, sucrose; N, NaCl; H, HCl; Q, quinine. Within-latency group connections are blue; between-latency group connections are red. Excitatory connections are solid lines; inhibitory connections are dashed lines.

Fig. 5.

Cross-correlograms and taste response profiles of cells with different types of functional connectivity. A: cross-correlation functions (CCFs) for each cell; shaded area indicates 99% confidence limit. B: taste response magnitudes for the source cell (solid line) and target cell (dashed line). C: raw electrophysiological records of each cell; A is the source and B is the target cell. D: results of principal component analyses of waveforms of cells shown in C.

Fig. 6.

Time course of paired-pulse attenuation in cells that showed early and late peak attenuation (n = 102). A: bimodal distribution of peak attenuation with modes at interpulse interval (IPI) of 10 ms and 50 ms. B: time course of attenuation in cells with early peak attenuation (≤20 ms) and late attenuation (≥30 ms).

Fig. 7.

A: mean + SE decay time in each latency group for cells that showed paired-pulse attenuation. B: mean + SE peak attenuation time in each latency group for cells that showed paired-pulse attenuation. Cells in the short-latency group that showed paired-pulse attenuation had significantly shorter decay time constants and peak attenuation times compared with cells in the medium-, medium-long-, and long-latency groups. **Short-latency groups are significantly different from all other groups with P < 0.01.

Fig. 8.

Location of cells recorded from the rostral NTS. A: illustration of coronal sections of the medulla showing the location of electrolytic lesions. ★, Taste-responsive cells; ▲, taste-responsive and non-taste-responsive cells; ●, non-taste-responsive cells. Numbers to right of each section indicate distance caudal to bregma. SpV, spinal nucleus of the trigeminal nerve. B: photomicrographs of representative lesions in the NTS. Dashed line indicates the border of the NTS. Bars at bottom right indicate 1.0 mm.

Fig. 9.

Model circuit diagram representing NTS functional connectivity superimposed on a stimulus-specific cell assembly model. Cells are organized into assemblies identified by their best stimulus. Black dots indicate cells. Solid lines connecting cells indicate excitatory connections; dashed lines indicate inhibitory connections. Arrows at the end of each line indicate the direction of the connection. Blue lines show connections within a latency group; red lines show connections across latency groups.

Fig. 10.

Timeline of proposed interactions among cells in different latency groups. Time is indicated by the arrow at left. At t = 0 the CT nerve is stimulated. Each column represents cells in a particular latency group. Placement along the timeline is approximate and meant to capture the average times of responses and/or interactions for all or some of the cells in each latency group. Blue circles are placed along the timeline at points where some cells in that latency group either contribute or receive activation. Red circles are placed at the mean time where cells in that latency group show evoked responses to CT nerve stimulation. Functional connections among cells within or across latency groups are indicated by lines connecting circles. The placement of those connections was determined by the average lag time of the peaks in the CCFs for each latency group. Solid red lines indicate excitatory connections; dashed blue lines indicate inhibitory connections. Each CT-evoked response initiates recurrent excitation among 1 or more groups of cells. See text for details.