Synaptic interactions due to convergent input from gustatory afferent fibers in the rostral nucleus of the solitary tract

1. Whole cell recordings from neurons in the rostral, gustatory nucleus of the solitary tract (rNST) were made using the ''blind'' patch-clamp technique in horizontal brain stem slices of rats. 2. Postsynaptic potentials (PSP) were elicited in 71 rNST neurons by electrical stimulation of the solitary tract (ST). To investigate PSPs evoked by convergent input from the chorda tympani and glossopharyngeal nerves, the ST was stimulated at levels where these two nerves terminate. These are referred to as rostral (rST) and intermediate (iST) ST, respectively. 3. When the rST was stimulated 72% of the PSPs were depolarizing, and 28% were hyperpolarizing (n = 64). Stimulation of the intermediate ST resulted in 75% depolarizing and 25% hyperpolarizing PSPs (n = 56). 4. Application of gamma-aminobuturic acid-A (GABA(A)) and glutamate receptor blockers revealed that all PSPs recorded in the present study were a composite of summed excitatory and inhibitory PSPs. Application of the GABA(A) receptor blocker bicuculline, by eliminating the hyperpolarizing component of a PSP, revealed the excitatory postsynaptic potential (EPSP) component of the potential. Bicuculline also increased the amplitude and prolonged the decay time of the depolarizing potentials once the hyperpolarizing potential component had been eliminated. These pure EPSP revealed by GABAA receptor blockade reversed at similar to 0 mV. 5. Application of glutamate ionotropic receptor blockers effectively eliminated the initiation of the synaptic responses evoked by ST stimulation. If the stimulus strength was increased, an inhibitory postsynaptic potential (IPSP) was elicited, presumably by direct activation of interneurons close to the stimulating electrode. These IPSPs had a mean reversal potential of -88 mV. 6. When synaptic responses were initiated by stimulation of the projection areas of both the chorda tympani and glossopharyngeal nerves, all neurons tested (n = 49) responded to stimulation of both sites on the ST. The resulting synaptic potential was a sum of the two individual synaptic potentials. 7. If stimulation of the rostral and intermediate sites both elicited depolarizing potentials, the potential resulting from stimulation of both sites was the arithmetical sum of the two individual PSPs. The EPSPs summed even if the time between stimulation of the rostral and intermediate sites was separated by less than or equal to 100 ms. 8. Inhibitory PSPs evoked by simultaneous stimulation of the rostral and intermediate ST also summed. The summation was not linear and saturated at a mean level of -66 mV. 9. When the PSP at one stimulation site was excitatory but inhibitory at the other site, the PSP wave form resulting from dual stimulation was a complex mixture of the two individual potentials. The inhibitory potential was capable of blocking action potentials resulting from the excitatory PSP. 10. These results indicate that synaptic responses in rNST are complex mixtures of excitatory and inhibitory potentials. The synaptic potentials result from excitatory afferent input mediated by glutamate and inhibitory input derived from interneurons. Inhibitory transmission is mediated primarily at GABA(A) synapses. Stimulation of the rNST afferent input derived from the chorda tympani and glossopharyngeal nerves reveals complex convergent input. The complexity of these synaptic interactions indicates that considerable processing of gustatory information occurs at the first central synapse in the taste pathway.