Effects of electrical stimulation of the chorda tympani nerve on taste responses in the nucleus of the solitary tract

Abstract

Despite evidence for an abundance of inhibitory synaptic processes within the taste-responsive portion of the brain stem, little is known about how these processes are activated or modulated. In this context, this study tested the hypothesis that activation of the chorda tympani nerve (CT) invokes inhibition that influences gustatory neural information processing in the rostral nucleus of the solitary tract (NTS). Stimulating electrodes were implanted in the middle ear of urethane-anesthetized rats to enable the passage of current across the CT. Electrophysiological responses to sucrose, NaCl, HCl, and quinine were recorded from single NTS neurons both individually and immediately following tetanic electrical stimulation of the CT. Additionally, NTS field responses to paired pulse stimulation of the CT were recorded. Electrical pulses delivered to the CT were found to produce a compound action potential with four components. Taste-responsive units in the NTS showed tetanus-evoked responses that varied in latency and strength. Those cells that showed strong, short latency responses to CT stimulation showed large magnitude responses to NaCl and were relatively narrowly tuned. Units with longer latencies generally responded more broadly to taste stimuli and with lower response magnitudes. Following tetanus, taste responses in 20 (43%) of the 46 units were reversibly altered in a stimulus-selective manner. Taste responses in 18 units were both enhanced and attenuated following tetanic stimulation, although attenuation was much more common. Additionally, tetanus was found to affect the temporal organization of spikes within taste responses to one stimulus in seven units (15%), four of which also showed changes in response magnitude to a different stimulus following tetanus. The influence of tetanus on taste responses was shown to be reliable and repeatable in neurons from which stimulus trials were recorded more than once. Across all units, responses to quinine were most dramatically and frequently attenuated following tetanus, while those to NaCl were least susceptible to change. NTS field responses evoked by paired pulse stimulation of the CT suggested that the initial pulse evoked an inhibitory influence in the NTS that decayed and returned to baseline by 2 s. These data are consistent with the idea that afferent input to the NTS normally activates inhibitory synaptic activity. As with other sensory systems, such inhibition may serve to facilitate contrast in the neural representation of different stimulus qualities.