The Journal of Neurophysiology Vol. 79 No. 2 February 1998, pp. 595-604
Copyright ©1998 The American Physiological Society

Tetanic Stimulation Induces Short-Term Potentiation of Inhibitory Synaptic Activity in the Rostral Nucleus of the Solitary Tract

Gintautas Grabauskas¹ and Robert M. Bradley^{1, 2}

¹ Department of Biologic and Materials Sciences, School of Dentistry; and ² Department of Physiology, Medical School, University of Michigan, Ann Arbor, Michigan 48109

Grabauskas, Gintautas and Robert M. Bradley. Tetanic stimulation induces short-term potentiation of inhibitory synaptic activity in the rostral nucleus of the solitary tract. J. Neurophysiol. 79: 595-604, 1998. 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 -aminobutyric acid-A (GABA_A) 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.

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