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

Anthony J A Molina, Michael P. Verzi, Andrea D. Birnbaum, Ebenezer N. Yamoah, Katherine Hammar, Peter J S Smith, Robert Paul Malchow

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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) eliminatedthe 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 neurones.

Original languageEnglish (US)
Pages (from-to)639-657
Number of pages19
JournalJournal of Physiology
Volume560
Issue number3
DOIs
StatePublished - Nov 1 2004

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Retinal Horizontal Cells
Neurotransmitter Agents
Glutamic Acid
Kainic Acid Receptors
Proton-Translocating ATPases
AMPA Receptors
Calcium-Transporting ATPases
Calcium
Retina
Calcium Compounds
6-Cyano-7-nitroquinoxaline-2,3-dione
Retinal Neurons
Excitatory Amino Acid Agonists
Sodium-Hydrogen Antiporter
Photolysis
Kainic Acid
Presynaptic Terminals
Microelectrodes
Protons
Sodium

ASJC Scopus subject areas

  • Physiology

Cite this

Molina, A. J. A., Verzi, M. P., Birnbaum, A. D., Yamoah, E. N., Hammar, K., Smith, P. J. S., & Malchow, R. P. (2004). Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate. Journal of Physiology, 560(3), 639-657. https://doi.org/10.1113/jphysiol.2004.065425

Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate. / Molina, Anthony J A; Verzi, Michael P.; Birnbaum, Andrea D.; Yamoah, Ebenezer N.; Hammar, Katherine; Smith, Peter J S; Malchow, Robert Paul.

In: Journal of Physiology, Vol. 560, No. 3, 01.11.2004, p. 639-657.

Research output: Contribution to journalArticle

Molina, AJA, Verzi, MP, Birnbaum, AD, Yamoah, EN, Hammar, K, Smith, PJS & Malchow, RP 2004, 'Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate', Journal of Physiology, vol. 560, no. 3, pp. 639-657. https://doi.org/10.1113/jphysiol.2004.065425
Molina, Anthony J A ; Verzi, Michael P. ; Birnbaum, Andrea D. ; Yamoah, Ebenezer N. ; Hammar, Katherine ; Smith, Peter J S ; Malchow, Robert Paul. / Neurotransmitter modulation of extracellular H+ fluxes from isolated retinal horizontal cells of the skate. In: Journal of Physiology. 2004 ; Vol. 560, No. 3. pp. 639-657.
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