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Reciprocal Interactions Between Calcium and Chloride in Rod Photoreceptors

¹ Department of Ophthalmology, University of Nebraska Medical Center, Omaha, Nebraska 68198; ² Department of Pharmacology, University of Nebraska Medical Center, Omaha, Nebraska 68198; ³ Department of General Zoology and Neurobiology, University of Pécs, H-7601 Pécs, Hungary

Submitted 17 October 2002; accepted in final form 22 April 2003

This study used imaging and electrophysiological techniques in salamander retinal slices to correlate Ca²⁺ and Cl^– levels in rods and thus test the hypothesis of a feedback interaction between Ca²⁺- and Ca²⁺-activated Cl^– channels whereby Cl^– efflux through Cl^– channels can inhibit Ca²⁺ channels. Increasing [K⁺]_o levels produced a concentration-dependent depolarization of rods accompanied by increases in [Ca²⁺]_i measured with Fura-2. The voltage dependence of increases in [Ca²⁺]_i was compared with the voltage dependence of the calcium current (I_Ca). [Cl^–]_i was measured with the dye, MEQ. Depolarization with high K⁺ to membrane potentials below –20 mV reduced [Cl^–]_i; larger depolarizations increased [Cl^–]_i. The Na/K/Cl cotransport inhibitor, bumetanide, shifted the apparent Cl^– equilibrium potential (E_Cl) to more negative potentials, suggesting that this cotransporter helps establish a relatively depolarized E_Cl. MEQ fluorescence changes evoked by high K⁺ were inhibited by niflumic acid (0.1 mM), NPPB (2 µM), or replacement of Ca²⁺ with Ba²⁺, suggesting that depolarization-evoked Cl^– changes result partly from stimulation of Ca²⁺-activated Cl^– channels. Replacing 12 mM [Cl^–]_o with CH₃SO₄^– produced a significant reduction in [Cl^–]_i. [Ca²⁺]_i increases evoked by 20 or 50 mM K⁺ were also significantly inhibited by replacing 12 mM [Cl^–]_o with CH₃SO₄^–. Thus modest depolarization can evoke increases in [Ca²⁺]_i that lead to reductions in [Cl^–]_i, and conversely, reductions in [Cl^–]_i inhibit depolarization-evoked [Ca²⁺]_i increases. These findings support the hypothesis that feedback interactions between Ca²⁺- and Ca²⁺-activated Cl^– channels may contribute to the regulation of presynaptic Ca²⁺ currents involved in synaptic transmission from rod photoreceptors.

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