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

Oct 24, 2002Visual neuroscience

D2-like dopamine receptors help calcium and chloride channels work together to reduce signal transfer from rod cells in the salamander retina

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Abstract

Quinpirole enhances L-type calcium currents in rods while simultaneously diminishing synaptic transmission.

Activation of D2-like dopamine receptors with quinpirole increases calcium-activated chloride currents in rod photoreceptors.
Quinpirole reduces rod input to second-order neurons in the tiger salamander retina without significantly changing rod voltage responses.
The enhancement of calcium currents by quinpirole is followed by chloride efflux that inhibits calcium signaling in rods.
Inhibition of chloride currents with niflumic acid prevents quinpirole from diminishing rod inputs to horizontal and bipolar cells.
The results indicate a complex interaction where initial increases in calcium currents lead to a negative feedback mechanism through chloride efflux.

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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-] 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+]i 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 approximately -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.

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

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