Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane

Abstract

1. In voltage clamped myelinated fibres, the K+ current was recorded in high-K+ media to allow analysis without complications due to K+ accumulation. 2. After a depolarization, the tail of K+ current following repolarization decreases in two phases: a fast phase lasting about 20 msec and a slow exponential phase lasting several hundred milliseconds. When the duration of the depolarization is increased, the amplitude at time zero of the fast phase increases (activation of the conductance) and then decreases slowly (inactivation of the conductance). Simultaneously, the amplitude of the slow phase, extrapolated to time zero of repolarization, increases slowly and reaches a steady-state level (about 20% of the maximum instantaneous current) after about 600 msec of depolarization. 3. The fast phase of the tail current is blocked by external application of 4-aminopyridine (4-AP) (KD = 10(-5)M). The slow phase is unaltered by 4-AP (10(-7)-10(-2)M). 4. In the presence of 4-AP (10-3M), the remaining slow K+ current, activated by depolarizations, does not inactivate. 5. During depolarizations and repolarizations, the conductance of the slow current (GKs) varies exponentially. The steady-state value of the slow conductance and its time constant of activation vary with voltage. The variation of the slow conductance with time and voltage can be described by a closed-open mode, assuming that each channel is gated by one particle. The activation kinetics of the slow current is unaltered by long lasting (500 msec) prepolarizations. 6. The fast K+ conductance, calculated from the fast tail current, is fully inactivated at the end of a 3 min depolarization to 0 mV. 7. The fast K+ conductance can be decomposed into two components: one component (GKf1) activating between -80 and -30 mV and inactivating very slowly (tau = 45 sec at E = 0 mV); one component (GKf2) activating between -40 mV and +30 mV and inactivating slowly (tau = 2 sec at E = 0 mV). t = 12 degrees C. 8. The maximum slow and fast conductances increase with [K]0. While the maximum fast conductance tends to saturate at high external K+ concentrations, the maximum slow conductance shows no sign of saturation. 9. A comparison between motor and sensory fibres shows that, while the amplitude of maximum slow and fast conductances are identical for both types of fibres, the amplitude of fast-1 conductance is larger and consequently the amplitude of fast-2 is smaller in motor than in sensory fibres. The different spike frequency adaptations observed on both types of fibres are discussed in relation to these different relative fast conductances amplitudes. 10. It is concluded that the K+ conductance of the nodal membrane is composed of three components (GKS, GKf1 and GKf2) corresponding to three different and distinct types of K+ channels.