D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina

Wallace B Thoreson, Salvatore L. Stella, Eric J. Bryson, John Clements, Paul Witkovsky

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

Activation of D2-like dopamine receptors in rods with quinpirole stimulates L-type calcium currents (ICa). This result appears inconsistent with studies showing that D2-like dopamine receptor activation diminishes rod signals in second-order retinal neurons. Since small reductions in [Cl-]i can inhibit photoreceptor ICa, we tested the hypothesis that enhancement of ICa, with the D2/D4 receptor agonist, quinpirole, increases calcium-activated chloride currents (ICl(Ca)) causing an efflux of Cl- from rods that would provide a negative feedback inhibition of ICa. In agreement with studies from Xenopus, quinpirole reduced rod input to second-order neurons of tiger salamander retina without significantly altering rod voltage responses. Quinpirole also diminished the amplitude of depolarization-evoked increases in [Ca2+], measured with Fura-2 in rods, a finding consistent with inhibition of synaptic transmission from rods. Electrophysiological and Cl--imaging experiments indicated ECl in rods is ∼ -20 mV. Quinpirole enhanced ICl(Ca) and elicited an efflux of Cl- at the resting potential. A similar Cl- efflux was produced by extracellular replacement of 24 mM Cl- with CH3SO4- and this low Cl- solution inhibited Ca2+responses to a similar degree as quinpirole did. When ICl(Ca) was inhibited with niflumic acid, quinpirole enhanced both ICa and depolarization-evoked increases in [Ca2+]i. Furthermore, with niflumic acid, quinpirole no longer inhibited rod inputs into horizontal and bipolar cells. These results suggest an initial enhancement of ICa by quinpirole is followed by a stimulation of Cl- currents, including ICl(Ca). The net result is a Cl- efflux that inhibits depolarization-evoked increases in [Ca2+]i and synaptic transmission from rods.

Original languageEnglish (US)
Pages (from-to)235-247
Number of pages13
JournalVisual Neuroscience
Volume19
Issue number3
DOIs
StatePublished - May 1 2002

Fingerprint

Quinpirole
Urodela
Calcium Chloride
Chloride Channels
Dopamine D2 Receptors
Calcium Channels
Retina
Niflumic Acid
Synaptic Transmission
Ambystoma
Retinal Neurons
Fura-2
Xenopus
Membrane Potentials
Calcium
Neurons

Keywords

  • Calcium current
  • Calcium-activated chloride current
  • Electrophysiology
  • Imaging
  • Outer retina

ASJC Scopus subject areas

  • Physiology
  • Sensory Systems

Cite this

D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina. / Thoreson, Wallace B; Stella, Salvatore L.; Bryson, Eric J.; Clements, John; Witkovsky, Paul.

In: Visual Neuroscience, Vol. 19, No. 3, 01.05.2002, p. 235-247.

Research output: Contribution to journalArticle

Thoreson, Wallace B ; Stella, Salvatore L. ; Bryson, Eric J. ; Clements, John ; Witkovsky, Paul. / D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina. In: Visual Neuroscience. 2002 ; Vol. 19, No. 3. pp. 235-247.
@article{0dc4929f662842ee8540f5278f189bbd,
title = "D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina",
abstract = "Activation of D2-like dopamine receptors in rods with quinpirole stimulates L-type calcium currents (ICa). This result appears inconsistent with studies showing that D2-like dopamine receptor activation diminishes rod signals in second-order retinal neurons. Since small reductions in [Cl-]i can inhibit photoreceptor ICa, we tested the hypothesis that enhancement of ICa, with the D2/D4 receptor agonist, quinpirole, increases calcium-activated chloride currents (ICl(Ca)) causing an efflux of Cl- from rods that would provide a negative feedback inhibition of ICa. In agreement with studies from Xenopus, quinpirole reduced rod input to second-order neurons of tiger salamander retina without significantly altering rod voltage responses. Quinpirole also diminished the amplitude of depolarization-evoked increases in [Ca2+], measured with Fura-2 in rods, a finding consistent with inhibition of synaptic transmission from rods. Electrophysiological and Cl--imaging experiments indicated ECl in rods is ∼ -20 mV. Quinpirole enhanced ICl(Ca) and elicited an efflux of Cl- at the resting potential. A similar Cl- efflux was produced by extracellular replacement of 24 mM Cl- with CH3SO4- and this low Cl- solution inhibited Ca2+responses to a similar degree as quinpirole did. When ICl(Ca) was inhibited with niflumic acid, quinpirole enhanced both ICa and depolarization-evoked increases in [Ca2+]i. Furthermore, with niflumic acid, quinpirole no longer inhibited rod inputs into horizontal and bipolar cells. These results suggest an initial enhancement of ICa by quinpirole is followed by a stimulation of Cl- currents, including ICl(Ca). The net result is a Cl- efflux that inhibits depolarization-evoked increases in [Ca2+]i and synaptic transmission from rods.",
keywords = "Calcium current, Calcium-activated chloride current, Electrophysiology, Imaging, Outer retina",
author = "Thoreson, {Wallace B} and Stella, {Salvatore L.} and Bryson, {Eric J.} and John Clements and Paul Witkovsky",
year = "2002",
month = "5",
day = "1",
doi = "10.1017/S0952523802192017",
language = "English (US)",
volume = "19",
pages = "235--247",
journal = "Visual Neuroscience",
issn = "0952-5238",
publisher = "Cambridge University Press",
number = "3",

}

TY - JOUR

T1 - D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina

AU - Thoreson, Wallace B

AU - Stella, Salvatore L.

AU - Bryson, Eric J.

AU - Clements, John

AU - Witkovsky, Paul

PY - 2002/5/1

Y1 - 2002/5/1

N2 - Activation of D2-like dopamine receptors in rods with quinpirole stimulates L-type calcium currents (ICa). This result appears inconsistent with studies showing that D2-like dopamine receptor activation diminishes rod signals in second-order retinal neurons. Since small reductions in [Cl-]i can inhibit photoreceptor ICa, we tested the hypothesis that enhancement of ICa, with the D2/D4 receptor agonist, quinpirole, increases calcium-activated chloride currents (ICl(Ca)) causing an efflux of Cl- from rods that would provide a negative feedback inhibition of ICa. In agreement with studies from Xenopus, quinpirole reduced rod input to second-order neurons of tiger salamander retina without significantly altering rod voltage responses. Quinpirole also diminished the amplitude of depolarization-evoked increases in [Ca2+], measured with Fura-2 in rods, a finding consistent with inhibition of synaptic transmission from rods. Electrophysiological and Cl--imaging experiments indicated ECl in rods is ∼ -20 mV. Quinpirole enhanced ICl(Ca) and elicited an efflux of Cl- at the resting potential. A similar Cl- efflux was produced by extracellular replacement of 24 mM Cl- with CH3SO4- and this low Cl- solution inhibited Ca2+responses to a similar degree as quinpirole did. When ICl(Ca) was inhibited with niflumic acid, quinpirole enhanced both ICa and depolarization-evoked increases in [Ca2+]i. Furthermore, with niflumic acid, quinpirole no longer inhibited rod inputs into horizontal and bipolar cells. These results suggest an initial enhancement of ICa by quinpirole is followed by a stimulation of Cl- currents, including ICl(Ca). The net result is a Cl- efflux that inhibits depolarization-evoked increases in [Ca2+]i and synaptic transmission from rods.

AB - Activation of D2-like dopamine receptors in rods with quinpirole stimulates L-type calcium currents (ICa). This result appears inconsistent with studies showing that D2-like dopamine receptor activation diminishes rod signals in second-order retinal neurons. Since small reductions in [Cl-]i can inhibit photoreceptor ICa, we tested the hypothesis that enhancement of ICa, with the D2/D4 receptor agonist, quinpirole, increases calcium-activated chloride currents (ICl(Ca)) causing an efflux of Cl- from rods that would provide a negative feedback inhibition of ICa. In agreement with studies from Xenopus, quinpirole reduced rod input to second-order neurons of tiger salamander retina without significantly altering rod voltage responses. Quinpirole also diminished the amplitude of depolarization-evoked increases in [Ca2+], measured with Fura-2 in rods, a finding consistent with inhibition of synaptic transmission from rods. Electrophysiological and Cl--imaging experiments indicated ECl in rods is ∼ -20 mV. Quinpirole enhanced ICl(Ca) and elicited an efflux of Cl- at the resting potential. A similar Cl- efflux was produced by extracellular replacement of 24 mM Cl- with CH3SO4- and this low Cl- solution inhibited Ca2+responses to a similar degree as quinpirole did. When ICl(Ca) was inhibited with niflumic acid, quinpirole enhanced both ICa and depolarization-evoked increases in [Ca2+]i. Furthermore, with niflumic acid, quinpirole no longer inhibited rod inputs into horizontal and bipolar cells. These results suggest an initial enhancement of ICa by quinpirole is followed by a stimulation of Cl- currents, including ICl(Ca). The net result is a Cl- efflux that inhibits depolarization-evoked increases in [Ca2+]i and synaptic transmission from rods.

KW - Calcium current

KW - Calcium-activated chloride current

KW - Electrophysiology

KW - Imaging

KW - Outer retina

UR - http://www.scopus.com/inward/record.url?scp=0036558474&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0036558474&partnerID=8YFLogxK

U2 - 10.1017/S0952523802192017

DO - 10.1017/S0952523802192017

M3 - Article

C2 - 12392173

AN - SCOPUS:0036558474

VL - 19

SP - 235

EP - 247

JO - Visual Neuroscience

JF - Visual Neuroscience

SN - 0952-5238

IS - 3

ER -