Potassium channel family in giant motor axons of Aglantha digitale

Abstract

1. The simplicity of the jellyfish nervous system makes it an ideal preparation to assess the contributions of different ion channels to behavior. In the giant motor axons of the jellyfish Aglantha digitale, low-threshold spikes elicit slow swimming, whereas escape swimming depends on a higher-threshold, overshooting sodium-dependent action potential. At least three kinetically distinct transient potassium channels (fast, intermediate, and slow) are concerned with spike management in this preparation. 2. In situ recording with patch-clamp micropipettes from clusters of potassium channels provides a means of studying their properties in isolation. The three classes of ion channel were identified in ensemble current averages by their kinetics, their response to a conditioning prepulse and their voltage dependence. All three were highly selective for potassium, and the reversal potential of their unitary currents depended on the level of potassium used to fill the patch pipette. 3. A single potassium permeability coefficient (PK) calculated from the Goldman, Hodgkin, Katz “constant field” equation was used to fit unitary current data from all three channels in concentrations of external potassium < or = 500 mM. 4. Data from ensemble tail currents in seawater indicated that the sodium permeability coefficient (PNa) of channels with either intermediate or slow kinetics was < or = 0.015 PK; preliminary data from channels with fast kinetics suggested that they too had a PNa/PK selectivity of approximately 0.01. 5. We propose that spike management in the giant motor axons of Aglantha depends on three members of a family of potassium-selective ion channels that seem likely to be structurally related.