Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat

Abstract

Electrical stimulation of the chorda tympani nerve (CT; innervating taste buds on the rostral tongue) is known to initiate recurrent inhibition in cells in the nucleus of the solitary tract (NTS, the first central relay in the gustatory system). Here, we explored the relationship between inhibitory circuits and the breadth of tuning of taste-responsive NTS neurons. Initially, NTS cells with evoked responses to electrical stimulation of the CT (0.1 ms pulses; 1 Hz) were tested with each of four tastants (0.1 M NaCl, 0.01 M HCl, 0.01 M quinine and 0.5 M sucrose) in separate trials. Next, the CT was electrically stimulated using a paired-pulse (10-2000 ms interpulse interval; blocks of 100 trials) paradigm. Forty-five (30 taste-responsive) of 51 cells with CT-evoked responses (36 taste-responsive) were tested with paired pulses. The majority (34; 75.6%) showed paired-pulse attenuation, defined as fewer evoked spikes in response to the second (test) pulse compared with the first (conditioning) pulse. A bimodal distribution of the peak of paired-pulse attenuation was found with modes at 10 ms and 50 ms in separate groups of cells. Cells with early peak attenuation showed short CT-evoked response latencies and large responses to relatively few taste stimuli. Conversely, cells with late peak attenuation showed long CT-evoked response latencies and small taste responses with less selectivity. Results suggest that the breadth of tuning of an NTS cell may result from the combination of the sensitivities of peripheral nerve inputs and the recurrent influences generated by the circuitry of the NTS.

Figure 1

Frequency distribution of latencies of evoked response to electrical stimulation of the CT nerve in all NTS cells recorded (n = 51). Black bars indicate taste-responsive cells; gray bars indicate non-taste-responsive cells.

Figure 2

Effects of paired pulse stimulation of the CT nerve in one cell. A. Paired-pulse enhancement at an interpulse interval of 30 ms. More spikes occurred in response to the test pulse compared with the conditioning pulse. B. Paired-pulse attenuation at an interpulse interval of 50 ms. Fewer spikes occurred in response to the test pulse compared with the conditioning pulse. Each panel shows oscilloscope tracings of 100 sweeps superimposed.

Figure 3

Frequency distribution of peak time of paired-pulse attenuation. Peak attenuation is defined as the interpulse interval at which the greatest percent decrement in the number of evoked pulses occurred between the conditioning and test pulses. Overall there was a bimodal distribution, especially for taste-responsive cells; however, for non-taste-responsive cells, the distribution was skewed toward longer interpulse intervals. Black bars indicate taste-responsive cells; gray bars indicate non-taste-responsive cells.

Figure 4

Time course of paired pulse attenuation in NTS cells that showed early and late peak attenuation. Shown is the percent difference (± SEM) in the number of evoked spikes in response to CT nerve stimulation following the conditioning pulse compared with the test pulse at various interpulse intervals. Cells with early peak attenuation show short lived time-dependent inhibition but cells with later peak attenuation show a gradual decline in time-dependent inhibition. Black bars show cells with early peak attenuation (≤ 20 ms); gray bars show cells with late peak attenuation (≥ 30 ms).

Figure 5

Distribution of “best taste stimuli” among cells that showed early and late peak attenuation. Cells with early peak attenuation showed the greatest paired pulse attenuation at IPIs ≤ 20 ms and are indicated with black bars. Cells with late peak attenuation showed the greatest paired pulse attenuation at IPIs ≥ 30 ms and are indicated by gray bars. The best taste stimulus was defined as the tastant that evoked the largest response among those tastants tested.

Figure 6

Location of cells recorded from the rostral NTS. A. Drawing of coronal sections of the brainstem showing the sites of electrolytic lesions indicating the location of NTS cells from which data were collected. Symbols are: star, taste-responsive cells; triangle, taste-responsive and non-taste-responsive cells recorded from approximately the same location; circle, non-taste-responsive cells. Numbers on upper right of drawing of each section indicate distance caudal to bregma. Abbreviations are: NTS, nucleus of the solitary tract; SpV, spinal nucleus of the trigeminal nerve. B. Photomicrographs of rostral NTS lesions showing the location of one NTS cell. Dotted line surrounds the NTS. Bars on lower right of each panel indicate 1.0 mm.