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¹ Department of Biology, Indiana Wesleyan University, Marion, IN 46953
² BioCurrents Research Center, Program in Molecular Physiology, Marine Biological Laboratory, Woods Hole, MA 02543
³ Department of Pharmacology and Experimental Therapeutics, Tufts University School of Medicine, Boston, MA 02111
⁴ Obesity Research Center, Evans Department of Medicine, Boston University School of Medicine, Boston, MA 02111
⁵ Department of Biological Sciences and Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, IL 60607
⁶ Division of Integrative Organismal Systems, National Science Foundation, Arlington, VA 22230

Correspondence to M.A. Kreitzer: matthew.kreitzer{at}indwes.edu

Self-referencing H⁺-selective microelectrodes were used to measure extracellular proton fluxes from cone-driven horizontal cells isolated from the retina of the catfish (Ictalurus punctatus). The neurotransmitter glutamate induced an alkalinization of the area adjacent to the external face of the cell membrane. The effect of glutamate occurred regardless of whether the external solution was buffered with 1 mM HEPES, 3 mM phosphate, or 24 mM bicarbonate. The AMPA/kainate receptor agonist kainate and the NMDA receptor agonist N-methyl-D-aspartate both mimicked the effect of glutamate. The effect of kainate on proton flux was inhibited by the AMPA/kainate receptor blocker CNQX, and the effect of NMDA was abolished by the NMDA receptor antagonist DAP-5. Metabotropic glutamate receptor agonists produced no alteration in proton fluxes from horizontal cells. Depolarization of cells either by increasing extracellular potassium or directly by voltage clamp also produced an alkalinization adjacent to the cell membrane. The effects of depolarization on proton flux were blocked by 10 µM nifedipine, an inhibitor of L-type calcium channels. The plasmalemma Ca^2+/H⁺ ATPase (PMCA) blocker 5(6)-carboxyeosin also significantly reduced proton flux modulation by glutamate. Our results are consistent with the hypothesis that glutamate-induced extracellular alkalinizations arise from activation of the PMCA pump following increased intracellular calcium entry into cells. This process might help to relieve suppression of photoreceptor neurotransmitter release that results from exocytosed protons from photoreceptor synaptic terminals. Our findings argue strongly against the hypothesis that protons released by horizontal cells act as the inhibitory feedback neurotransmitter that creates the surround portion of the receptive fields of retinal neurons.

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