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

Abstract

SUMMARY1. 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+ (9 mM), 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-pyridine (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 (PC/0PK) 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+.

Antagonists of the cGMP‐gated conductance of vertebrate rods block the photocurrent in scallop ciliary photoreceptors.

“…This discrepancy has been attributed in part to a negative feedback mechanism, by which a reduction of Ca2+ influx caused by blockage of light-sensitive channels lowers [Ca2+]i and activates guanylate cyclase, so that the resulting elevation of cGMP levels leads to recruitment of extra 'spare' channels and restoration of the dark current (Haynes, 1992). A scheme of this nature would not be expected to operate effectively in the present case, because the light-sensitive conductance of Pecten ciliary photoreceptor is selective for K+ ions, with no significant permeation by divalent cations (Gomez & Nasi, 1994a), and the contribution of other Ca2+-permeable channels (Cornwall & Gorman, 1979) would be eliminated by voltage clamping.…”

Calcium-Independent, cGMP-Mediated Light Adaptation in Invertebrate Ciliary Photoreceptors

“…those found in other species), the light response of ciliary photoreceptors is wholly decoupled from any detectable change in [Ca] i , at least over the duration of the interval monitored (500 ms), which is substantially longer than the time constant for adaptation to set in (Gomez and Nasi, 1997). It is true that these cells are capable of generating Ca-dependent action potentials (Cornwall and Gorman, 1979), but those occur at the termination of a light stimulus and are responsible for triggering the well known defensive "shadow reflex" (Hartline, 1938). No contribution of depolarization-activated calcium channels in altering cytosolic Ca is therefore expected in the dark (because of steady-state inactivation at V rest , which is approximately Ϫ35 mV), nor during illumination, when the membrane potential hyperpolarizes.…”

Colour dependence of the early receptor potential and late receptor potential in scallop distal photoreceptor

“…The dual optical stimulator was the same as that used previously (Cornwall & Gorman, 1979), with the following exceptions. For studies on the early receptor potential (e.r.p.…”

“…The preparation, dissection, perfusion system, and flow chamber for holding the preparation have been described previously (Cornwall & Gorman, 1979). The ionic composition of the various artificial sea water (ASW) solutions is given in the preceding paper (Cornwall & Gorman, 1983).…”

“…8B and McReynolds & Gorman, 1970 a;Cornwall & Gorman, 1979). It was suggested previously (Cornwall &(Gorman, 1979) that the small action potentials are initiated at some electrically distant site in the axon by the after-depolarization and are electrotonically conducted back toward the recording site in the receptor cell body. The plot in Fig.…”