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Modulation of extracellular proton fluxes from retinal horizontal cells of the catfish by depolarization and glutamate

Modulation of extracellular proton fluxes from retinal horizontal cells of the catfish by depolarization and glutamate
Modulation of extracellular proton fluxes from retinal horizontal cells of the catfish by depolarization and glutamate
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 microM 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
0022-1295
169-182
Kreitzer, Matthew A.
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Collis, Leon P.
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Molina, Anthony J.A.
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Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Malchow, Robert Paul
8328c125-23da-41c6-87a2-5cb642ea2a79
Kreitzer, Matthew A.
5807387c-ed8f-4f5d-8008-2fa3ed91a6cf
Collis, Leon P.
66f825a3-f4a7-4e85-a1ca-ee16497b8a81
Molina, Anthony J.A.
a2324f63-c696-4517-825e-1394ee76b573
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Malchow, Robert Paul
8328c125-23da-41c6-87a2-5cb642ea2a79

Kreitzer, Matthew A., Collis, Leon P., Molina, Anthony J.A., Smith, Peter J.S. and Malchow, Robert Paul (2007) Modulation of extracellular proton fluxes from retinal horizontal cells of the catfish by depolarization and glutamate. The Journal of General Physiology, 130 (2), 169-182. (doi:10.1085/jgp.200709737). (PMID:17664345)

Record type: Article

Abstract

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 microM 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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Published date: August 2007
Organisations: University of Southampton

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Local EPrints ID: 188749
URI: http://eprints.soton.ac.uk/id/eprint/188749
ISSN: 0022-1295
PURE UUID: 4934fe67-97b7-4929-92c7-dcf0a6df95a9
ORCID for Peter J.S. Smith: ORCID iD orcid.org/0000-0003-4400-6853

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Date deposited: 01 Jun 2011 10:29
Last modified: 05 Nov 2019 01:41

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Author: Matthew A. Kreitzer
Author: Leon P. Collis
Author: Anthony J.A. Molina
Author: Robert Paul Malchow

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