Contribution of calcium and potassium permeability changes to the off response of scallop hyperpolarizing photoreceptors

Abstract

1. The membrane response of the distal photoreceptors in the retina of the scallop Pectin irradians to the termination of a bright white light (off response) is shown to be composed of the decay of the hyperpolarizing receptor potential and an action potential with slow kinetics. 2. The action potential can be produced in darkness in the absence of external Na+ ions by membrane depolarization. 3. The action potential is maintained by replacement of external Ca2+ with Sr2+ or Ba2+, but not by Mg2+. In normal external Ca2+ (9mM), the action potential is abolished by the addition of the Ca2+ inhibitors, La3+, Co2+, and Mn2+ or the organic Ca2+ antagonist D-600. 4. Elevated external Ca2+ concentrations increase the rate of rise and peak amplitude of the action potential as well as the rate of repolarization and after hyperpolarization, but decrease the duration. 5. The rate of rise and peak amplitude of the action potential are increased by the K+ antagonists tetraethylammonium (TEA) 4-amino-phyridine (4-AP), Ba2+ and procaine. The antagonists have different effects on subsequent phases of the response, however. External TEA and Ba2+ increase the duration, but decrease the rate of repolarization and abolish the after hyperpolarization, whereas external 4-AP and procaine increase the rate of repolarization, decrease the duration and increase the after hyperpolarization. 6. The ratio of the Ca2+ to K+ permeability (P Ca/P K) estimated from the constant field equation at the peak of the action potential in different external Ca2+ concentrations is close to 1. 7. The maximum rate of rise and the peak amplitude of the action potential are increased by membrane hyperpolarization and decreased by membrane depolarization. They are decreased by background light intensity relative to their value in the dark. 8. In normal ASW the action potential can be identified during the off response as a small overshoot of membrane potential relative to its value in the dark. 9. The rate of repolarization of the off response in normal ASW is reduced by agents or conditions which inhibit or reduce Ca2+ permeability changes, e.g. external Co2+ and La2+ or zero external Ca2+. 10. Our results suggest that a voltage-dependent increase in membrane permeability to Ca2+ and to K+ ions modifies the repolarizing phase of the receptor potential.