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Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate

Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate
Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate
Self-referencing H+-selective microelectrodes were used to measure extracellular H+ fluxes from horizontal cells isolated from the skate retina. A standing H+ flux was detected from quiescent cells, indicating a higher concentration of free hydrogen ions near the extracellular surface of the cell as compared to the surrounding solution. The standing H+ flux was reduced by removal of extracellular sodium or application of 5-(N-ethyl-N-isopropyl) amiloride (EIPA), suggesting activity of a Na+–H+ exchanger. Glutamate decreased H+ flux, lowering the concentration of free hydrogen ions around the cell. AMPA/kainate receptor agonists mimicked the response, and the AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) eliminated the effects of glutamate and kainate. Metabotropic glutamate agonists were without effect. Glutamate-induced alterations in H+ flux required extracellular calcium, and were abolished when cells were bathed in an alkaline Ringer solution. Increasing intracellular calcium by photolysis of the caged calcium compound NP-EGTA also altered extracellular H+ flux. Immunocytochemical localization of the plasmalemma Ca2+–H+-ATPase (PMCA pump) revealed intense labelling within the outer plexiform layer and on isolated horizontal cells. Our results suggest that glutamate modulation of H+ flux arises from calcium entry into cells with subsequent activation of the plasmalemma Ca2+–H+-ATPase. These neurotransmitter-induced changes in extracellular pH have the potential to play a modulatory role in synaptic processing in the outer retina. However, our findings argue against the hypothesis that hydrogen ions released by horizontal cells normally act as the inhibitory feedback neurotransmitter onto photoreceptor synaptic terminals to create the surround portion of the centre-surround receptive fields of retinal neurone
0022-3751
639-657
Molina, Anthony J.A
32c67502-2bb3-4283-8dd4-9301821c9eb7
Verzi, Michael P.
7b71c7ba-af11-407f-8801-a6368221e8c8
Birnbaum, Andrea D.
6bd34d84-3ea8-40d7-9d17-14b29a457a38
Yamoah, Ebenezer N.
78da5e87-c125-449f-b8c0-b15624dfc45d
Hammar, Katherine
c1706f67-2af6-4246-9c7f-341d48a693ec
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Malchow, Robert Paul
b0b1afa6-0f50-488c-9028-7f05d1932ee1
Molina, Anthony J.A
32c67502-2bb3-4283-8dd4-9301821c9eb7
Verzi, Michael P.
7b71c7ba-af11-407f-8801-a6368221e8c8
Birnbaum, Andrea D.
6bd34d84-3ea8-40d7-9d17-14b29a457a38
Yamoah, Ebenezer N.
78da5e87-c125-449f-b8c0-b15624dfc45d
Hammar, Katherine
c1706f67-2af6-4246-9c7f-341d48a693ec
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Malchow, Robert Paul
b0b1afa6-0f50-488c-9028-7f05d1932ee1

Molina, Anthony J.A, Verzi, Michael P., Birnbaum, Andrea D., Yamoah, Ebenezer N., Hammar, Katherine, Smith, Peter J.S. and Malchow, Robert Paul (2004) Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate. The Journal of Physiology, 560 (3), 639-657. (doi:10.1111/(ISSN)1469-7793). (PMID:15272044)

Record type: Article

Abstract

Self-referencing H+-selective microelectrodes were used to measure extracellular H+ fluxes from horizontal cells isolated from the skate retina. A standing H+ flux was detected from quiescent cells, indicating a higher concentration of free hydrogen ions near the extracellular surface of the cell as compared to the surrounding solution. The standing H+ flux was reduced by removal of extracellular sodium or application of 5-(N-ethyl-N-isopropyl) amiloride (EIPA), suggesting activity of a Na+–H+ exchanger. Glutamate decreased H+ flux, lowering the concentration of free hydrogen ions around the cell. AMPA/kainate receptor agonists mimicked the response, and the AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) eliminated the effects of glutamate and kainate. Metabotropic glutamate agonists were without effect. Glutamate-induced alterations in H+ flux required extracellular calcium, and were abolished when cells were bathed in an alkaline Ringer solution. Increasing intracellular calcium by photolysis of the caged calcium compound NP-EGTA also altered extracellular H+ flux. Immunocytochemical localization of the plasmalemma Ca2+–H+-ATPase (PMCA pump) revealed intense labelling within the outer plexiform layer and on isolated horizontal cells. Our results suggest that glutamate modulation of H+ flux arises from calcium entry into cells with subsequent activation of the plasmalemma Ca2+–H+-ATPase. These neurotransmitter-induced changes in extracellular pH have the potential to play a modulatory role in synaptic processing in the outer retina. However, our findings argue against the hypothesis that hydrogen ions released by horizontal cells normally act as the inhibitory feedback neurotransmitter onto photoreceptor synaptic terminals to create the surround portion of the centre-surround receptive fields of retinal neurone

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Published date: 2004
Organisations: University of Southampton

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Local EPrints ID: 188829
URI: http://eprints.soton.ac.uk/id/eprint/188829
ISSN: 0022-3751
PURE UUID: 0956d3dd-1b85-4b68-b6c8-f1338bb4475f
ORCID for Peter J.S. Smith: ORCID iD orcid.org/0000-0003-4400-6853

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Date deposited: 06 Jun 2011 08:48
Last modified: 15 Mar 2024 03:38

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Contributors

Author: Anthony J.A Molina
Author: Michael P. Verzi
Author: Andrea D. Birnbaum
Author: Ebenezer N. Yamoah
Author: Katherine Hammar
Author: Robert Paul Malchow

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