Response latency to lingual taste stimulation distinguishes neuron types within the geniculate ganglion

Abstract

The purpose of this study was to investigate the role of response latency in discrimination of chemical stimuli by geniculate ganglion neurons in the rat. Accordingly, we recorded single-cell 5-s responses from geniculate ganglion neurons (n = 47) simultaneously with stimulus-evoked summated potentials (electrogustogram; EGG) from the anterior tongue to signal when the stimulus contacted the lingual epithelium. Artificial saliva served as the rinse solution and solvent for all stimuli [(0.5 M sucrose, 0.03-0.5 M NaCl, 0.01 M citric acid, and 0.02 M quinine hydrochloride (QHCl)], 0.1 M KCl as well as for 0.1 M NaCl +1 μM benzamil. Cluster analysis separated neurons into four groups (sucrose specialists, NaCl specialists, NaCl/QHCl generalists and acid generalists). Artificial saliva elevated spontaneous firing rate and response frequency of all neurons. As a rule, geniculate ganglion neurons responded with the highest frequency and shortest latency to their best stimulus with acid generalist the only exception. For specialist neurons and NaCl/QHCl generalists, the average response latency to the best stimulus was two to four times shorter than the latency to secondary stimuli. For NaCl-specialist neurons, response frequency increased and response latency decreased systematically with increasing NaCl concentration; benzamil significantly decreased NaCl response frequency and increased response latency. Acid-generalist neurons had the highest spontaneous firing rate and were the only group that responded consistently to citric acid and KCl. For many acid generalists, a citric-acid-evoked inhibition preceded robust excitation. We conclude that response latency may be an informative coding signal for peripheral chemosensory neurons.

Fig. 1.

Raw electrophysiological traces from individual gustatory neurons in response to 0.5 M sucrose, 0.1 M NaCl, 0.01 M citric acid, 0.02 M QHCl, and 0.1 M KCl.

Fig. 2.

Dendrogram showing the results of the hierarchical cluster analysis. Next to each neuron is the capital letter indicating the taste stimulus (S, 0.5 M sucrose; N, 0.1 NaCl; A, 0.01 M citric acid; Q, 0.02 M QHCl) that evoked the best response, followed by small letter(s) indicating taste stimuli that evoked a significant response indicated by the Poisson distribution.

Fig. 3.

Responses by each neuron to 0.5 M sucrose, 0.1 M NaCl, 0.01 M citric acid, 0.02 M QHCl, and 0.01 M KCl. Within each group, neurons were arranged by response (spike/s relative to baseline) to the best stimulus in descending order from left to right.

Fig. 4.

Mean response latencies (milliseconds) and percentage of neurons (by group) responding (excitation or inhibition) to the 4 basic taste stimuli and to 0.1 M KCl as indicated by the Poisson distribution.

Fig. 5.

Mean baseline and response frequency (spike/s) by each neuron group to the 4 basic taste stimuli and to 0.1 M KCl. ∗, significance (P < 0.01).

Fig. 6.

Mean responses (spike/s) by inhibitory (▪, n = 3) and noninhibitory (, n = 6) acid-generalist neurons to stimulation with 0.01 M citric acid for 5 s. ∗ and gray star, within group significance (P < 0.05), corresponding to inhibitory and noninhibitory acid generalists, respectively. †, between group significance (P < 0.05).

Fig. 7.

Mean response frequency (spike/s relative to baseline) and response latency (milliseconds) to 4 concentrations of NaCl (0.03–0.5 M) for each neuron group. ∗, significant differences (P < 0.05) in response frequency from the adjacent lower concentration. Gray star, significant differences (P < 0.05) in response latency from the adjacent lower concentration.

Fig. 8.

Mean response frequency (spike/s relative to baseline) and response latency (milliseconds) to 0.1 M NaCl presented alone twice before and once after presentation of NaCl mixed with 1 μM benzamil for each neuron group. ∗, the response frequency to NaCl + benzamil is significantly different (P < 0.001) from 0.1 M NaCl alone. Gray star, the response latency to NaCl + benzamil is significantly different (P < 0.01) from 0.1 M NaCl alone.