Visual adaptation modulates a potassium conductance in retinular cells of the crayfish

Abstract

Crayfish photoreceptors exhibit a voltage-dependent potassium conductance, GK, that is generally similar to the delayed rectifier channel described in neurons and other arthropod retinular cells. GK activation (i.e. the apparent threshold, Vth) occurs near the resting potential and GK is substantially reduced by 25 mM extracellular tetraethylammonium (TEA) and by intracellular Cs+ injections. Light exposure, sufficient to reduce visual sensitivity 100-fold, increases Vth (shifts it in the depolarizing direction) by about 20 mV. The light-dependent change in Vth does not depend upon the corresponding increase (depolarization) of the steady-state membrane potential nor does it depend upon inward calcium currents. Vth is slightly influenced by fluctuations in Ko associated with the light-elicited currents. During light exposure Ko (measured with K+-sensitive electrodes) increases by 2.1 mM (equivalent to an 8 mV increase in EK). This increase in EK makes only a modest contribution to the light-dependent change in Vth as determined by perfusion with high potassium salines. Intracellular calcium injections increase Vth by 10 to 20 mV and reduce visual sensitivity by 5- to 10-fold. The results imply that during exposure to high levels of illumination, K+ currents at the steady-state membrane potential are diminished by a calcium-dependent change in GK gating and, to a smaller degree, by a reduced K+ concentration gradient. It is notable that Ca2+ appears to inhibit both GK and the light-elicited conductance from both inside and outside the plasma membrane. As a consequence of the light-dependent change in Vth, GK makes only modest contributions to the changes in sensitivity and speed normally associated with light adaption. These functions are regulated by the transduction pathway and are revealed at the resting potential in the time course and magnitude of the light-elicited currents.