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Participation of Kv1 Channels in Control of Membrane Excitability and Burst Generation in Mesencephalic V Neurons

Department of Physiological Science, University of California at Los Angeles, Los Angeles, California

Submitted 19 September 2008; accepted in final form 5 January 2009

Abstract

The function and biophysical properties of low threshold Kv1 current in control of membrane resonance, subthreshold oscillations, and bursting in mesencephalic V neurons (Mes V) were examined in rat brain stem slices (P8–P12) using whole cell current and voltage patch-clamp methods. -dendrotoxin application, a toxin with high specificity for Kv1.1, 1.2, and 1.6 channels, showed the presence of a low-threshold K⁺ current that activated rapidly around –50 mV and was relatively noninactivating over a 1-s period and had a V_1/2max of –36.2 mV. Other toxins, specific for individual channels containing either Kv 1.1, 1.2, or 1.3 -subunits, were applied individually, or in combination, and showed that Kv1 channels are heteromeric, composed of combinations of subunits. In current-clamp mode, toxin application transformed the high-frequency resonant properties of the membrane into a low-pass filter and concomitantly reduced the frequency of the subthreshold membrane oscillations. During this period, rhythmical bursting was transformed into low-frequency tonic discharge. Interestingly, in a subset of neurons that did not show bursting, low doses of -dendrotoxin (-DTX) sufficient to block 50% of the low threshold Kv1 channels induced bursting and increased the resonant peak impedance and subthreshold oscillations, which was replicated with computer simulation. This suggests that a critical balance between inward and outward currents is necessary for bursting. This was replicated with computer simulation. Single cell RT-PCR and immunohistochemical methods confirmed the presence of Kv1.1, 1.2, and 1.6 -subunits in Mes V neurons. These data indicate that low threshold Kv1 channels are responsible for membrane resonance, contribute to subthreshold oscillations, and are critical for burst generation.