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 tasteresponsive) 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.

Synaptic characteristics of rostral nucleus of the solitary tract neurons with input from the chorda tympani and glossopharyngeal nerves

“…Similar subsets of neurons that have higher cut-off frequencies that pass the afferent input relatively unchanged have been described in the caudal NST (Mifflin, 2001) and also in the paired pulse study of CT-rNST synapses (Rosen and DiLorenzo, 2009). …”

“…A more recent similar study of second order rNST neurons to paired pulse stimulation of the CT reported frequency dependent synaptic depression (Rosen and DiLorenzo, 2009). In this in vivo study rNST neurons were isolated and responses to tongue stimulation with chemicals determined and then responses of the same neurons were measured to paired pulse stimulation of the CT at pulse intervals ranging from 10 to 2000 ms (i.e.…”

“…The results of this in vivo study are comparative to the intracellular recordings in the current study and demonstrate frequency dependent changes of transmission across the first central synapse in the taste pathway. The authors of the in vivo study while noting that although frequency dependent depression might account for their result, concluded that inhibitory processes are the most likely contributing factor (Rosen and DiLorenzo, 2009). Since we used GABA A synaptic blockers to eliminate inhibitory activity it is more likely that the paired pulse depression was the result of the frequency dependent depression characteristics of the CT-rNST neuron synapses.…”

“…The fact that time dependent depression occurs in vivo indicates that it is of significance in transmission of information between the peripheral and central taste pathways. The time course of the paired pulse depression was correlated with the breadth of tuning of the chemosensitive rNST neurons and the low pass filtering speculated to stabilize the temporal pattern of the afferent input (Rosen and DiLorenzo, 2009). Alternatively, the low pass filtering may isolate the input to frequencies that are in the linear part of the response concentration function thereby enhancing the ability to distinguish differences in stimulus concentration.…”

Enhancing GABAergic Tone in the Rostral Nucleus of the Solitary Tract Reconfigures Sensorimotor Neural Activity

“…Moreover, application of the GABA antagonist bicuculline can broaden the breadth of tuning of taste-responsive rNTS cells. Moreover, inhibitory interactions in rNTS may enhance and stabilize the temporal structure of taste-evoked spike trains (Rosen and Di Lorenzo, 2009). The caveat to what is known about the functionality of GABA-driven inhibition in neural coding of taste is that it is all derived from studies in anesthetized subjects; the function of inhibition in taste coding in awake subjects may be different.…”