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 Scopus citations

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
Publication statusPublished - May 1 2002

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Keywords

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

ASJC Scopus subject areas

  • Physiology
  • Sensory Systems

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