Characterization of a voltage-gated K+ channel that accelerates the rod response to dim light

doi:10.1016/0896-6273(89)90267-5

Neuron

Volume 3, Issue 5, November 1989, Pages 573-581

https://doi.org/10.1016/0896-6273(89)90267-5 Get rights and content

Abstract

In this study a K⁺ current, I_Kx, in isolated salamander rod photoreceptors was characterized and its role in shaping small photovoltages was examined. I_Kx is a standing outward current of about 40 pA at −30 mV that deactivates slowly when the cell is hyperpolarized (τ_max = 0.25 s). The voltage and time dependence of I_Kx are similar to that of M-current, but I_Kx can be distinguished from M-current because it is not suppressed by acetylcholine and is “blocked” by external Ba²⁺ in a surprising manner: the activation range of I_Kx is shifted strongly in the positive direction. Using current-clamp recordings and a computer simulation of the photo-response, we show that I_Kx figures prominently in setting the dark resting potential and accelerates the voltage response to small photocurrents.

References (36)

C.M. Armstrong et al.
Interaction of barium ions with potassium channels in squid giant axons
Biophys. J.
(1980)
M.B. Bellhorn et al.
Localization of ions in retina by secondary ion mass spectrometry
Exp. Eye Res.
(1976)
D.A. Brown
M-currents: an update
Trends Neurosci.
(1988)
G.L. Fain et al.
Membrane conductances of photoreceptors
Prog. Biophys. Mol. Biol.
(1981)
H.F. Leeper et al.
Mixed rod-cone responses in horizontal cells of snapping turtle retina
Vis. Res.
(1979)
A.V. Maricq et al.
Calcium and calciumdependent chloride currents generate action potentials in solitary cone photoreceptors
Neuron
(1988)
W.G. Owen et al.
Ionic studies of vertebrate rods
Curr. Top. Membr. Trans.
(1981)
W.G. Owen et al.
High-pass filtering of small signals by retinal rods
Biophys. J.
(1983)
J.A. Ward et al.
Hydrogen ion effects and the vertebrate late receptor potential
Biochim. Biophys. Acta
(1972)
P.R. Adams et al.
M-currents and other potassium currents in bullfrog sympathetic neurones
J. Physiol.
(1982)

D. Attwell

Ion channels and signal processing in the outer retina

Quart. J. Exp. Physiol.

(1986)

D. Attwell et al.

Behavior of the rod network in tiger salamander retina mediated by properties of individual rods

J. Physiol.

(1980)

D. Attwell et al.

The properties of single cones isolated from the tiger salamander retina

J. Physiol.

(1982)

D. Attwell et al.

Signal clipping by the rod output synapse

Nature

(1987)

C.R. Bader et al.

A voltage-clamp study of the light response in solitary rods of the tiger salamander

J. Physiol.

(1979)

C.R. Bader et al.

Voltageactivated and calcium-activated currents studied in solitary rod inner segments from the salamander retina

J. Physiol.

(1982)

S. Barnes et al.

Ionic channels of the inner segment of tiger salamander cone photoreceptors

J. Gen. Physiol.

(1989)

D.A. Baylor et al.

Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina

J. Physiol.

(1977)

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^∗: Present address: Department of Medical Physiology, University of Calgary Faculty of Medicine, 3330 Hospital Drive NW, Calgary, Alberta, Canada T2N 4N1.

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Neuron

ArticleCharacterization of a voltage-gated K+ channel that accelerates the rod response to dim light

Abstract

Biophys. J.

Exp. Eye Res.

Trends Neurosci.

Prog. Biophys. Mol. Biol.

Vis. Res.

Neuron

Curr. Top. Membr. Trans.

Biophys. J.

Biochim. Biophys. Acta

M-currents and other potassium currents in bullfrog sympathetic neurones

J. Physiol.

Ion channels and signal processing in the outer retina

Quart. J. Exp. Physiol.

Behavior of the rod network in tiger salamander retina mediated by properties of individual rods

J. Physiol.

The properties of single cones isolated from the tiger salamander retina

J. Physiol.

Signal clipping by the rod output synapse

Nature

A voltage-clamp study of the light response in solitary rods of the tiger salamander

J. Physiol.

Voltageactivated and calcium-activated currents studied in solitary rod inner segments from the salamander retina

J. Physiol.

Ionic channels of the inner segment of tiger salamander cone photoreceptors

J. Gen. Physiol.

Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina

J. Physiol.

Article
Characterization of a voltage-gated K⁺ channel that accelerates the rod response to dim light