Blockage of the light-sensitive conductance in hyperpolarizing photoreceptors of the scallop: Effects of tetraethylammonium and 4-aminopyridine

Abstract

The tight-seal whole-cell recording technique was used to examine the effect of tetraethylammonium (TEA) and 4-aminopyridine (4-AP) on the photocurrent of hyperpolarizing ciliary photoreceptors isolated from the distal retina of the bay scallop (Pecten irradians). In these cells, light causes an increase in a conductance that is highly selective to potassium ions. Extracellular application of TEA at a concentration of 50 mM produced a modest, reversible block (≈ 35% at -20 mV holding potential). The blockage was weakly voltage dependent, increasing by ∼20% for a 20-mV hyperpolarization, suggestive of a site of interaction superficially located within the electric field of the membrane. Treatment with TEA produced no significant changes either in the light sensitivity of the photocurrent or in its kinetics. The effects of superfusion with 4-AP were more dramatic: the light-evoked current was nearly abolished (> 95%) at submillimolar concentrations, with a half-maximal dose of ∼0.6 μm. The blockage had a rapid onset and was slowly reversible. No significant use or voltage dependency were observed. A number of control experiments indicated that the phototransduction cascade remained functional during treatment with 4-AP: the early receptor current, the prolonged aftercurrent and its suppression, the photoresponse kinetics and the light sensitivity of the cell were little affected by 4-AP, suggesting that the suppression of the photocurrent is due to blockage of the light-sensitive channels, rather than impairment of some of the activation steps. The results are discussed in the light of a possible kinship between the light-activated potassium channels of invertebrate hyperpolarizing photoreceptors and the family of rapidly-inactivating voltage-dependent potassium channels, which typically exhibit high susceptibility to blockage by this drug.