Comparison of the serotonin-sensitive and Ca(2+)-activated K+ channels in Aplysia sensory neurons

1. Single potassium channel currents were recorded in cell-attached and cell-free patches from Aplysia sensory neurons. Two prominent classes of K+ channels were identified that have similar single-channel current amplitude at 0 mV: (1) the resting conductance serotonin-sensitive K+ channels (S-channels) previously described in these neurons; and (2) a calcium-activated K+ channel. A series of experiments were carried out which enable these channels to be distinguished on the basis of their biophysical properties. These experiments also provide further insight into the gating and ionic selectivity of the S-channel. 2. In inside-out patches, single calcium-activated K+ channel currents (IK,Ca) show a linear i-V curve with a slope conductance of 66 pS (normal sea water outside, 360 mM-KCl inside) whereas single S-channels display an outwardly rectifying i-V curve with a slope conductance of 90 pS at 0 mV. 3. The gating of IK,Ca has a steep voltage dependence, with open probability showing an e-fold increase for a 16 mV depolarization. Increasing internal calcium concentration from 0.2 to 10 microM shifts the activation curve by 60 mV in the hyperpolarizing direction. 4. S-channel gating is independent of internal calcium (from less than 10 nM up to 100 microM). Steady-state open probability of the S-channel generally shows a weak dependence on membrane potential, with open probability increasing twofold for a 30-100 mV depolarization. Occasional patches were observed with S-channels displaying a much greater voltage sensitivity, with open probability increasing e-fold for a 16-20 mV depolarization. 5. S-channels are selective for K+ over Na+. The selectivity ratio depends on the ratio of Na+ to K+ concentration on the same side of the membrane. Increasing K+ concentration appears to increase relative Na+ permeability, suggesting ion-ion interactions within the channel. 6. We conclude that Aplysia sensory neurons contain two prominent distinguishable classes of K+ channels, the Ca(2+)-independent S-channel and a Ca(2+)-activated channel. The gating properties of the S-channels allow them to contribute outward repolarizing current over a wide range of membrane potentials so that their modulation by neurotransmitters contributes to changes in both resting potential and action potential duration.