Ca2+ flux in retinal rod and cone outer segments: differences in Ca2+ selectivity of the cGMP-gated ion channels and Ca2+ clearance rates

Abstract

In intact rod and cone photoreceptors of various vertebrate species, depolarization in the dark to > or = +20 mV specifically activates the cGMP-dependent conductance in the outer segment. This activation reflects a voltage-dependent decrease in cytoplasmic Ca2+ and the consequent activation of a Ca(2+)-dependent guanylyl cyclase. The conductance activation in cones is much faster in time course and larger in extent than that in rods. Simulations of the experimental results suggest that these differences arise from differences in Ca2+ homeostasis in the rod and cone outer segments. Direct measurements demonstrate that, indeed, the Ca2+ permeability of the cGMP-gated channels is higher in cones than in rods. Also, as was previously known, the rate of Ca2+ efflux from cone outer segments is higher than that in rods. Therefore, a given light-dependent change in membrane current should cause a much larger and much quicker decrease in Ca2+ concentration in cones than in rods. The activity of every Ca(2+)-dependent biochemical event in the outer segment should, hence, change more rapidly and to a larger extent in cones than in rods. We propose that these kinetic and stoichiometric differences in the function of Ca(2+)-dependent processes is important in explaining the difference in the transduction signal of the two receptor types.