Properties of ion channels closed by light and opened by guanosine 3',5'‐cyclic monophosphate in toad retinal rods.

Abstract

SUMMARY1. In patch-clamp recordings from outer segments of dark-adapted rod photoreceptors, single-channel recordings were obtained from the light-sensitive conductance when divalent cations were omitted from the pipette solution bathing the extracellular face of the recorded patch of membrane.2. Activity of the light-sensitive channel was suppressed by light within the normal response range of the dark-adapted rod. During dim, steady illumination, the rate of opening of the channel fluctuated dramatically, as expected qualitatively from statistical fluctuations in the number of photoisomerizations occurring within the effective collecting area of the recorded patch.3. The light-sensitive channel flickered rapidly in the open state, so that individual events appeared as a burst of openings and closings. The average duration of a burst was 0-78+0-03 ms (mean+ s.E.). The average duration of an individual opening was 0 18 + 0008 ms. The average closed duration within a burst was 0-37 + 0-02 ms.4. Hyperpolarization of the recorded patch had no effect on average burst or open duration, although opening frequency increased slightly (+ 18-6 + 4-9%; n = 13; mean+ S.E.). Average single-channel current increased linearly with hyperpolarization, giving an estimated single-channel conductance of 20-5 + 1F1 pS. By extrapolation of the relation between channel current and hyperpolarization, the dark driving force was estimated to be about 48 mV.5. In addition to reducing the rate of channel events, dim non-saturating light also reduced the average duration of a burst of openings and the average duration of openings within a burst.6. About 50 % of cell-attached patches showed no channel activity in darkness.

The light-sensitive conductance of hyperpolarizing invertebrate photoreceptors: a patch-clamp study.

“…These recordings were presumably made possible by the favorable geometry of the ciliary appendages, which is less formidable than in Lima. The unitary conductance of light-sensitive channels is significantly smaller than that of the primary light-sensitive channels of depolarizing receptors (Bacigalupo and Lisman, 1983;Nagy and Stieve, 1990;Nasi and Gomez, 1992), and is similar to the conductance of light-suppressed single-channel currents in amphibian rods, measured in the absence of divalent cations (Matthews and Watanabe, 1987).…”

Cyclic AMP-induced slow inward current in depolarized neurons of Aplysia californica

“…None of the above pharmacological effects on the inverting element of the medial cell response appear to be related to the concomitant disappearance in those cells of the CAMP-sensitive K conductance, as shown by the demonstration of the same effects on the inverting response in medial cells in which the noninverting element has first been eliminated by blocking all K conductances with an intracellular injection of cesium. The CAMP-induced slow inward current described here resembles, in many respects, that activated by cGMP in the photoreceptors (Fesenko et al, 1985;Haynes et al, 1986;Zimmerman and Baylor, 1986;Matthews and Watanabe, 1987) by both CAMP and cGMP in olfactory receptor cilia (Nakamura and Gold, 1987), and by CAMP in cardiac myocytes (Egan et al, 1988). In all of these cases (see Hockberger and Swandulla, 1987), findings from whole-cell experiments performed in normal internal and external solutions reveal an outwardly rectifying current that is carried primarily by Na ions passing through a rather nonselective cationic channel, as attested by a reversal potential that is in each case inferior to ENa.…”

“…One of these nucleotide-induced responses, seen as early as 1975 by Liberman et al, is a TTX-, ouabain-, and amiloride-insensitive slow inward current that is correlated with an increase in intracellular Na (Aldenhoff et al, 1983;Connor and Hockberger, 1984a) and disappears when extracellular Na is replaced by Tris (Kononenko et al, 1983;Connor and Hockberger, 1984a;Swandulla and Lux, 1984), TMA (Aldenhoff et al, 1983;Connor and Hockberger, 1984a), saccharose (Aldenhoff et al, 1983), bis-tris propane (Connor and Hockberger, 1984a), mannitol (Kehoe, 1985a), or glucosamine (Hara et al, 1985), but persists when Na is replaced by lithium (Aldenhoff et al, 1983;Connor and Hockberger, 1984a;Hara et al, 1985). A similar nucleotideinduced current has recently been described in photoreceptors (Fesenko et al, 1985;Haynes et al, 1986;Matthews and Watanabe, 1987) olfactory receptor cilia (Nakamura and Gold, 1987), and myocytes (Egan et al, 1988). In molluscan neurons, this Na-sensitive response is characterized by its selective activation by CAMP (see, however, Connor and Hockberger, 1984a), its sensitivity to external Ca (Aldenhoff et al, 1983;Hara et al, 1985;Kehoe, 1985a; but see also Kononenko et al, 1983), its atypical voltage dependence (Kononenko, 198 1;Connor and Hockberger, 1984a;Hara et al, 1985;Kehoe, 1985a;Gillette and Green, 1987; but see also Kononenko et al, 1983), and its enhancement by intracellular acidification (Aldenhoff et al, 1983;Green and Gillette, 1988).…”

Blockage and permeation of divalent cations through the cyclic GMP‐activated channel from tiger salamander retinal rods.

“…It is now generally believed that the light-sensitive channel in vertebrate photoreceptors is identical to the membrane channel activated by cyclic GMP (Caretta & Cavaggioni, 1983;Fesenko, Kolesnikov & Lyubarsky, 1985;Yau & Nakatani, 1985;Matthews & Watanabe, 1987;Kaupp, Niidome, Tanabe, Terada, B6nigk, Stiihmer, Cook, Kangawa, Matsuo, Hirose, Miyata & Numa, 1989;Yau & Baylor, 1989) and so the two different terms will be used interchangeably. The selectivity of this channel to monovalent and divalent cations and their interaction has been studied in intact rods by changing solutions at the extracellular side of the cell (Yau & Nakatani, 1984;Hodgkin, McNaughton & Nunn, 1985;Nakatani & Yau, 1988a;.…”