Making time count: functional evidence for temporal coding of taste sensation

Abstract

Although the temporal characteristics of neural responses have been proposed as a mechanism for sensory neural coding, there has been little evidence thus far that this type of information is actually used by the nervous system. Here the authors show that patterned electrical pulses trains that mimic the response to the taste of quinine can produce a bitterlike sensation when delivered to the nucleus tractus solitarius of behaving rats. Following conditioned aversion training using either "quinine simulation" patterns of electrical stimulation or natural quinine (0.1 mM) as a conditioned stimulus, rats specifically generalized the aversion to 2 bitter tastants: quinine and urea. Randomization of the quinine simulation patterns resulted in generalization patterns that resembled those to a perithreshold concentration (0.01 mM) of quinine. These data provide strong evidence that the temporal pattern of brainstem activity may convey information about taste quality and underscore the functional significance of temporal coding.

Figure 1

(A) Temporal patterns of electrical stimulation. Graph showing the temporal arrangement of electrical pulses in all quinine simulation patterns (Q1–Q5), the composite pattern (C) and their randomized controls (Q1r–Q5r and Cr). (B) Interpulse interval (IPI) histograms for each of the six patterns and their randomized control patterns. For each quinine simulation pattern, the histogram for the randomized counterpart was identical by definition.

Figure 2

Number of licks for all quinine simulation patterns in Experiment 1A. Mean number of licks (±SEM) for water baseline (no electrical stimulation) and for all lick-contingent quinine simulation patterns (Q1–Q5) and their randomized counterparts (Q1r-Q5r) in 10-min testing sessions. All rats drank plain water.

Figure 3

Number of licks for the composite quinine simulation pattern in Experiment 1B. Mean number of licks (±SEM) for water baseline (no electrical stimulation) and for the lick-contingent composite quinine simulation pattern and its randomized counterpart, randomized composite. All rats drank plain water.

Figure 4

Proportion of licks (mean ± SEM) show the conditioned stimulus, either electrical stimulation or natural quinine, for all groups. C = composite; Cr = randomized composite; 0.01 Q = 0.01 mM quinine; 0.1 Q, 0.1 mM quinine.

Figure 5

Number of licks for generalization and extinction tests after conditioned aversion training using either quinine simulation patterns of NTS stimulation or 0.1-mM quinine as conditioned stimuli in Experiment 2. Mean number of licks (±SEM) for each of five tastants presented for 1 min, timed from the first lick, for the composite, Q1, and 0.1-mM quinine groups. Generalization tests (left) were given on the day after rats reached criterion for a conditioned aversion; extinction tests were given on the day after rats regained 90% of their baseline intake during lick-contingent electrical stimulation (only water presented) or 0.1 mM quinine depending on the group.

Figure 6

Number of licks for generalization and extinction tests following conditioned aversion training using either randomized quinine simulation patterns of NTS stimulation or 0.01 mM quinine as conditioned stimuli in Experiment 2. Details are as in Figure 4.

Figure 7

Number of licks for taste stimuli tested in the Naïve Control groups and for generalization and extinction tests following conditioned aversion training in the Histological Control group in Experiment 2. Rats in the Naïve Control group were unoperated and tested after being trained to lick water in the experimental chamber. Rats in the Histological Control group consisted of rats from all experimental groups with electrode placement outside of the NTS. All rats in this group learned a conditioned aversion but did not generalize the aversion to any of the taste stimuli tested.

Figure 8

Suppression ratios for generalization tests. Mean suppression ratio ± SEM for the pooled quinine simulation (Composite and Q1) and randomized quinine simulation (Randomized Composite and Q1r) are shown as filled and gray columns. Square symbols indicate the mean suppression ratio for the 0.1 mM quinine group and round symbols represent the mean suppression ratios for the 0.01 mM quinine group. Abbreviations for taste stimuli are: Q, quinine; N, NaCl; H, HCl; U, urea; S, sucrose.

Figure 9

Results of histological analyses for Experiments 1 and 2. Numbers in center of figure between drawings of brainstem sections refer to the distance in mm caudal to bregma. Line at lower left of each panel indicates 1 mm. A. Location of electrode tips for all rats in Experiment 1. B.-D. Location of electrode tips for all rats in Experiment 2 with the exception of placements in 5 animals in the Histological Control group. See text for details.