Potentiation of GABAergic synaptic transmission in the rostral nucleus of the solitary tract.

ABSTRACT

Whole-cell recordings were made from neurons in the rostral nucleus of the solitary tract in horizontal brainstem slices. Monosynaptic GABAA receptor-mediated inhibitory postsynaptic potentials were evoked by single stimulus shocks or by high-frequency tetanic stimulation in the presence of glutamate receptor blockers. While single stimulus-evoked inhibitory postsynaptic potentials had variable amplitudes, tetanic stimulation-induced, hyperpolarizing postsynaptic potentials were of a more constant amplitude. Furthermore, tetanic stimulation resulted in potentiation of the amplitude of single stimulus shock-evoked inhibitory postsynaptic potentials. Of 55 neurons that were tested, potentiation lasted over 30 min for 11, 10-30 min for 13, less than 10 min for 23 and no potentiation occurred in eight. Tetanic stimulation did not result in potentiation of the tetanic stimulus-evoked hyperpolarizing postsynaptic potentials. Both the single stimulus shock- and tetanic stimulus-evoked potentials had similar inhibition concentration-response curves to the GABAA antagonist, bicuculline methiodide (EC50 = 0.75 and 0.83, respectively), indicating that they were mediated by the same postsynaptic receptors. By comparing the effect of bicuculline methiodide on the amplitude of the single stimulus shock-evoked inhibitory postsynaptic potentials and the tetanic stimulus-evoked hyperpolarizing potentials, we concluded that a single stimulus shock does not activate all postsynaptic GABAA receptors. However, tetanic stimulation results in activation of all postsynaptic GABAA receptors and induces long-lasting changes in the presynaptic GABAergic neuron. These long-lasting changes of the presynaptic neuron facilitate the release of GABA during single stimulus shock and, as a consequence, more postsynaptic receptors are activated during single stimulus shock-evoked synaptic transmission. This conclusion is supported by the results of experiments in which the extracellular Ca2+ concentration was manipulated to change the amount of neurotransmitter released from the presynaptic GABAergic terminals. The single stimulus shock-evoked inhibitory postsynaptic potentials were sensitive to the extracellular Ca2+ concentration, whereas tetanic stimulus-evoked inhibitory post-synaptic potentials were essentially insensitive to extracellular Ca2+ concentration. The relationship between the single stimulus shock-evoked inhibitory postsynaptic potential amplitude and extracellular Ca2+ concentration indicates that, in control physiological saline containing 2.5 mM Ca2+, a single stimulus shock activates less than half the postsynaptic GABA receptors. The phenomenon of long-lasting potentiation of inhibitory transmission within the rostral nucleus of the solitary tract may be important in the processing of gustatory information and play a role in taste-guided behaviors.