The mechanism gated by external potassium and sodium controls the resting conductance in hippocampal and cortical neurons

Abstract

The excitation of densely packed mammalian central neurons is followed by a substantial transitory elevation of external K + concentration. This phenomenon may have a different functional significance depending on how the resting membrane conductance mechanisms react to the changes in the gradient of these ions. We have found that in the hippocampal and cortex neurons of rat a large fraction of the membrane conductance in the vicinity of the resting potential is provided by the K + permeability mechanism which is gated by external K + and Na +. The responses of acutely isolated pyramidal neurons to rapidly altered external [K +] were investigated using the whole-cell patch clamp and concentration clamp techniques. Elevation of [K +] out induced a biphasic inward current at membrane potentials more negative than the reversal potential for K + ions. This current consisted of an “instantaneously” increased leakage component and a slowly activated current (τ=48 ms at 21°C) designated below as I ΔK. The latter demonstrated a first order activation kinetics with a remarkably high Q 10=7.31. I ΔK was absent in the peripheral sensory neurons as well as in the Purkinje neurons. Slow activation of I ΔK was critically dependent on [Na +] out: substitution of the extracellular Na + with choline chloride or Li + led to the “instantaneous” reaction of the membrane to the changes in [K +] out. By slowing down potassium influx, I ΔK may be of importance in preserving densely packed pyramidal neurons from immediate excitation following rapid increases in [K +] out.