Tetanic stimulation induces short-term potentiation of inhibitory synaptic activity in the rostral nucleus of the solitary tract.

ABSTRACT

Whole cell recordings from neurons in the rostral nucleus of the solitary tract (rNST) were made to explore the effect of high-frequency tetanic stimulation on inhibitory postsynaptic potentials (IPSPs). IPSPs were elicited in the rNST by local electrical stimulation after pharmacological blockade of excitatory synaptic transmission. Tetanic stimulation at frequencies of 10-30 Hz resulted in sustained hyperpolarizing IPSPs that had a mean amplitude of -68 mV. The hyperpolarization resulted in a decrease in neuronal input resistance and was blocked by the gamma-aminobutyric acid-A (GABAA) antagonist bicuculline. For most of the neurons (n = 87/102), tetanic stimulation resulted in a maximum hyperpolarization immediately after initiation of the tetanic stimulation, but for some neurons the maximum was achieved after three or more consecutive shock stimuli in the tetanic train of stimuli. When the extracellular Ca2+ concentration was reduced, the maximum IPSP amplitude was reached after several consecutive shock stimuli in the tetanic train for all neurons. Tetanic stimulation at frequencies of 30 Hz and higher resulted in IPSPs that were not sustained but decayed to a more positive level of hyperpolarization. In some neurons the decay was sufficient to become depolarizing and resulted in a biphasic IPSP. It was possible to evoke this biphasic IPSP in all the neurons tested if the cells were hyperpolarized to -75 to -85 mV. The ionic mechanism of the depolarizing IPSPs was examined and was found to be due to an elevation of the extracellular K+ concentration and accumulation of intracellular Cl-. Tetanic stimulation increased the mean 80-ms decay time constant of a single shock-evoked IPSP up to 8 s. The length of the IPSP decay time constant was dependent on the duration and frequency of the tetanic stimulation as well as the extracellular Ca2+ concentration. Afferent sensory input to the rNST consists of trains of relatively high-frequency spike discharges similar to the tetanic stimulation frequencies used to elicit the IPSPs in the brain slices. Thus the short-term changes in inhibitory synaptic activity in the slice preparation probably occur in vivo and may play a key role in taste processing by facilitating synaptic integration.