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Firing properties and Na⁺-dependent plateau potentials of neurons in nucleus principalis trigemini of the gerbil Sandler, Vladislav Michael


We investigated the electrophysiological properties of neurons in the nucleus principalis trigemini (PrV), using whole-cell recordings in in vitro slice preparations of brainstem. We identified three groups mainly by their firing properties: type 1 neurons were spontaneously active and able to discharge action potentials in doublets or bursts; type 2 neurons, depolarized by current pulses, fired action potentials in a nonadapting (tonic) pattern; and the less commonly encountered type 3 neurons also fired in such patterns but with biphasic afterhyperpolarizations. Neurobiotin staining and reconstruction did not reveal significant morphological differences between types 1 and 2 neurons which were multipolar, with dendritic trees distributed mainly along one axis. Type 3 neurons had more expansive and circular dendritic arborizations. Hyperpolarization beyond -75 mV or down to the K⁺ reversal aotential due to current pulse injection, resulted in an inward rectification which was expressed as a sag in the voltage responses of types 1 and type 2 neurons. A rebound subthreshold depolarization or spike burst was evident on termination of a pulse. In type 1 neurons, the application of Cs⁺ (2 mM), a blocker of a hyperpolarization-activated cation current (l[sub H]), eliminated the voltage sag and the dependence of the rebound spike-latency on membrane voltage, but did not alter the main features of the rebound response. We attribute the inward rectification to the activation of an l[sub H]-like current. Depolarization by current pulse injection into type 1 neurons, hyperpolarized with DC to prevent firing, occasionally evoked "plateau potentials". This feature, not observed in types 2 or 3 neurons, consisted of an initial oscillatory burst of 3 or 4 spikes that decreased in amplitude, and then plateaued for a variable duration, followed by an abrupt repolarization. We always observed these voltage shapes on depolarizing current pulse injection during perfusion with Ca²⁺ free media, with or without the Ca²⁺-channel antagonists, Co²⁺ or Cd²⁺, and during external tetraethylammonium (TEA) application. An analysis of the depolarizing voltage responses evoked by current pulses in type 1 neurons during blockade of persistent and transient Na+ conductances with TTX (600 nM) and K⁺ conductances with TEA (10 mM) and 4-aminopyridine (4-AP; 0.5 mM), revealed the presence of inward rectification. This had a peak activation near the plateau itself and was completely blocked by Ni²⁺ (600 μM). These observations are consistent with the activation of a transient 2+-conductance. Hence, we propose that a Ca²⁺-dependent K⁺ conductance mechanism controls the generation of the plateau potential. The application of TTX, as low as 0.6 nM, increased the latency to onset and decreased the duration of the plateau potential, without greatly affecting action potentials. In a concentration-dependent manner, TTX enhanced the negative slope of the plateau, as it descended towards an abrupt terminal repolarization. Higher concentrations of TTX (e.g., 60 nM for 6 min) abolished the plateau potential before completely blocking action potential genesis. Low [Na⁺]-perfusion, however, simultaneously reduced the amplitudes of plateau potentials and fast spikes. Evidently, small changes in a persistent Na⁺ conductance can produce marked changes in firing behavior of type 1 neurons. A long-lasting hyperpolarization followed current pulses producing the plateau potential. Indeed, subthreshold or suprathreshold depolarization in Ca²⁺ free ACSF with Co²⁺ (1 mM) also evoked a hyperpolarization at the offset of the current pulse. This hyperpolarization was blocked by TTX (5 nM and 300 nM) and varied with changes in the duration of the plateau potential. A semiquantitative analysis revealed that the magnitude of the hyperpolarization depended on the neuronal depolarization. We conclude, therefore, that Na⁺ entry during a depolarization can increase a K⁺ conductance in type 1 neurons. From our studies, we conclude that plateau potentials represent the contributions of persistent and transient Na⁺ conductances, high threshold Ca²⁺-dependent rectification, as well as Ca²⁺- and Na⁺-dependent K⁺ conductances. The ability to fire bursts as part of Na+-dependent plateaus is an unusual property in neurons of primary sensory nuclei. In nucleus principalis trigemini, burst responses to mechanical stimuli represent a normal output of neurons that likely are subject to intra- and extracellular messenger regulation.

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