Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T18:33:17.109Z Has data issue: false hasContentIssue false
  • English
  • Français

Modulation of cone to horizontal cell transmission by Calcium and pH in the fish retina

Published online by Cambridge University Press:  02 June 2009

Krisztina Harsanyi  and
Stuart c. Mangel
Krisztina Harsanyi
Affiliation:
Departments of Ophthalmology and Physiology and Biophysics, and the Neurobiology Research Center, University of Alabama School of Medicine, Birmingham
Stuart c. Mangel
Affiliation:
Departments of Ophthalmology and Physiology and Biophysics, and the Neurobiology Research Center, University of Alabama School of Medicine, Birmingham
Get access Rights & Permissions [Opens in a new window]

Abstract

The effects of small changes in the calcium and sodium concentrations and in the pH of superfusion medium on the membrane potential and light-evoked responses of cone horizontal cells in the goldfish retina were examined. Conventional intracellular recording, a bicarbonate-based superfusion medium, and a specially designed superfusion apparatus that reduced pressure wave disturbances were used. An increase in the extracellular calcium concentration, [Ca2+]∘ from control levels (0.1 mM) to 1.0 mM hyperpolarized cone horizontal cells and reduced the magnitude of their light responses at all stimulus intensities. Addition of 20 mM NaCl to the 1.0 mM Ca2+ Ringer’s solution reversed the hyperpolarizing effect of the 1.0 mM Ca2+ but addition of 20 mM choline, a monovalent cation that does not pass through cyclic GMP-activated channels, did not. Reduction of the superfusate pH from 7.6 to 7.2 by switching from a Ringer’s solution gassed with 3% CO2 to one gassed with 10% CO2 hyperpolarized horizontal cells and reduced the magnitude of their light responses at all stimulus intensities for both 0.1 and 1.0 mM Ca,2+ Ringer’s solutions. An increase in pH to 8.2 by gassing the superfusate with 1% CO2 slightly depolarized the cells in 0.1 mM Ca2+ Ringer’s solution but slightly hyperpolarized the cells in the 1.0 mM Ca2+ Ringer’s solution. Following pharmacological isolation of the horizontal cells from synaptic input with high doses of glutamate (4–5 mM) and/or Co2+ (4 mM) treatment, no effect on horizontal cell membrane potential due to changes in pH or [Ca2+]∘ was observed. These findings are discussed with respect to the cellular mechanisms and sites of action in the outer retina that are affected by changes in pH∘ and [Ca2+]∘.

Keywords

RetinaHorizontal cellspHCalcium
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 1 , January 1993 , pp. 81 - 91
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allee, W.C., Finkel, A.J. & Hoskins, W.H. (1940). The growth of goldfish in homotypically conditioned water; a population study in mass physiology. Journal of Experimental Zoology 84, 417–443.CrossRefGoogle Scholar
Ariel, M., Lasater, E.M., Mangel, S.C. & Dowling, J.E. (1984). On the sensitivity of HI horizontal cells of the carp retina to glutamate, aspartate and their agonists. Brain Research 295, 179–183.CrossRefGoogle Scholar
Augustine, G.J., Charlton, M.P. & Smith, S.J. (1987). Calcium action in synaptic transmitter release. Annual Review of Neuroscience 10, 633–693.Google Scholar
Balestrino, M. & Somjen, G.G. (1988). Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat. Journal of Physiology (London) 396, 247–266.CrossRefGoogle ScholarPubMed
Barnes, S. & Bui, Q. (1991). Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors. Journal of Neuroscience 11, 4015–4023.CrossRefGoogle ScholarPubMed
Bentley, P.J. (1971). Endocrines and Osmoregulation: A Comparative Account of the Regulation of Water and Salt in Vertebrates. New York: Springer-Verlag, pp. 199–210.Google Scholar
Borgula, G.A., Karwoski, C.J. & Steinberg, R.H. (1989). Light-evoked changes in extracellular pH in frog retina. Vision Research 29, 1069–1077.Google Scholar
Borgula, G.A. & Steinberg, R.H. (1984). Light-evoked changes of [H+]∘ in the retina of the intact cut eye. Investigative Ophthalmology and Visual Science (Suppl.) 25, 406.Google Scholar
Burnside, B. & Nagle, B. (1983). Retinomotor movements of photo-receptors and retinal pigment epithelium: Mechanisms and regulation. Progress in Retinal Research 2, 67–110.Google Scholar
Cervetto, L. & Piccolino, M. (1974). Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science 183, 417–419.CrossRefGoogle ScholarPubMed
Chesler, M. (1990). The regulation and modulation of pH in the nervous system. Progress in Neurobiology 34, 401–427.CrossRefGoogle ScholarPubMed
Christensen, B.N. & Hida, E. (1990). Protonation of histidine groups inhibits gating of the quisqualate/kainate channel protein in isolated catfish cone horizontal cells. Neuron 5, 471–478.Google Scholar
Copenhagen, D.R. & Takahashi, K.-I. (1991). Evidence that Na+/H+ and Cl−/HCO−3 exchangers regulate the intracellular pH of retinal horizontal cells. Investigative Ophthalmology and Visual Science (Suppl.) 32, 992.Google Scholar
Corey, D.P., Dubinsky, J.M. & Schwartz, E.A. (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. Journal of Physiology 354, 557–575.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopa-mine and second messengers. Journal of Physiology 414, 351–375.CrossRefGoogle Scholar
Dowling, J.E., Lasater, E.M., Van Buskirk, R. & Watling, K.J. (1983). Pharmacological properties of isolated fish horizontal cells. Vision Research 23, 421–432.Google Scholar
Dowling, J.E. & Ripps, H. (1971). S-potential in the skate retina: intracellular recordings during light and dark adaption. Journal of General Physiology 58, 163–189.CrossRefGoogle Scholar
Dowling, J.E. & Ripps, H. (1973). Effect of magnesium on horizontal cell activity in the skate retina. Nature 242, 101.CrossRefGoogle ScholarPubMed
Gallemore, R.P. & Steinberg, R.H. (1988). Light-evoked changes in [Ca2+]∘ in chick retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 104.Google Scholar
Gedney, C. & Ostroy, S.E. (1978). Hydrogen ion effects of the vertebrate photoreceptor: The pK’s of ionizable group affecting cell permeability. Archives of Biochemistry and Biophysics 188, 105–113.CrossRefGoogle ScholarPubMed
Gold, G.H. & Korenbrot, J.I. (1980). Light-induced calcium release by intact retinal rods. Proceedings of the National Academy of Sciences of the U.S.A. 77, 5557–5561.Google Scholar
Hankinson, K.C. & Rowe, J.S. (1983). Evidence for low calcium in the subretinal space of the dark-adapted goldfish. Journal of Physiology 345, 68P.Google Scholar
Hille, B. (1992). Ionic Channels of Excitable Membranes. Sunderland, Massachusetts: Sinauer Associates, Inc.Google Scholar
Hodgkin, A.L., McNaughton, P.A. & Nunn, B.J. (1985). The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. Journal of Physiology 358, 447–468.Google Scholar
Kaila, K., Voipio, J. & Akerman, E.O. (1984). Free extracellular [Ca2+] at photoreceptor level equals that in vitreous in frog and carp eyes. Investigative Ophthalmology and Visual Science (Suppl). 25, 1395–1401.Google ScholarPubMed
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar and amacrine cells in the goldfish retina. Journal of Physiology 207, 623–633.CrossRefGoogle ScholarPubMed
Katz, B. (1969). The Release of Neural Transmitter Substances. Liverpool, England: Liverpool University Press.Google Scholar
Kleinschmidt, J. (1990). High pH sensitivity of photoreceptor synaptic transmission. Investigative Ophthalmology and Visual Science (Suppl). 31, 388.Google Scholar
Knapp, A.G. & Dowling, J. (1987). Dopamine enhances excitatory amino acid gated conductances in retinal horizontal cells. Nature (London) 325, 437–439.Google Scholar
Krafte, D.S. & Kass, R.S. (1988). Hydrogen ion modulation of Ca channel current in cardiac ventricular cells. Journal of General Physiology 91, 641–657.CrossRefGoogle ScholarPubMed
Kraig, R.P., A-Filho, C.R.Ferreir & Nicholson, C. (1983). Alkaline and acid transients in cerebellar microenvironment. Journal of Neurophysiology 49, 831–850.CrossRefGoogle ScholarPubMed
Laufer, M. (1982). Electrophysiological studies of drug actions on horizontal cells. In The S-Potential, ed. Drujan, B. & Laufer, M., pp. 257–279. New York: Alan R. Liss, Inc.Google Scholar
Liebman, P.A., Mueller, P. & Pugh, E.N. (1984). Protons suppress the dark current of frog retinal rods. Journal of Physiology 347, 85–110.Google Scholar
Linsenmeier, R.A. (1986). Effects of light and darkness on oxygen distribution and consumption in the cat retina. Journal of General Physiology 88, 521–542.CrossRefGoogle ScholarPubMed
Livsey, C.T., Huang, B., Xu, J. & Karwoski, C.J. (1990). Light-evoked changes in extracellular calcium concentration in frog retina. Vision Research 30, 853–861.CrossRefGoogle ScholarPubMed
Llinas, R., Steinberg, I.Z. & Walton, K. (1976). Presynaptic calcium currents and relation to synaptic transmission: Voltage clamp study in squid giant synapse and theoretical model for calcium gate. Proceedings of the National Academy of Sciences of the U.S.A. 73, 2918–2922.CrossRefGoogle ScholarPubMed
Lockwood, A.P.M. (1961). Ringer solutions and some notes on the physiological basis of their ionic composition. Comparative Biochemistry and Physiology 2, 241–289.Google Scholar
Mangel, S.C., Ariel, M. & Dowling, J.E. (1985). Effects of acidic amino acid antagonists upon the spectral responses of carp horizontal cells: Circuitry of the outer retina. Journal of Neuroscience 5, 2839–2850.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science (Washington) 229, 1107–1109.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform-horizontal cell system of the fish retina: Effects of dopamine, light stimulation and time in the dark. Proceedings of the Royal Society B (London) 231, 91–121.Google ScholarPubMed
Mangel, S.C. & Harsanyi, K. (1992). Dopamine affects the membrane potential of horizontal cells presynaptically in a pH-dependent manner. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1406.Google Scholar
Marc, R.E. & Lam, E.M.K. (1981). Uptake of aspartic and glutamic acid by photoreceptors in goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 78, 7185–7189.CrossRefGoogle ScholarPubMed
Matthews, H.R., Fain, G.L., Murphy, R.L.W. & Lamb, T.D. (1990). Light adaptation in cone photoreceptors of the salamander: A role for cytoplasmic calcium. Journal of Physiology 420, 447–469.CrossRefGoogle ScholarPubMed
Meyertholen, E.P., Wilson, M.J. & Ostroy, S.E. (1986). The effects of HEPES, bicarbonate and calcium on the cGMP content of vertebrate rod photoreceptors and the isolated electrophysiological effects of cGMP and calcium. Vision Research 26, 521–533.CrossRefGoogle ScholarPubMed
Miki, N., Baraban, J.M., Keirns, J.J., Boyce, J.J. & Bitensky, M.W. (1975). Purification and properties of the light-activated cyclic nucleotide phosphodiesterase of rod outer segments. Journal of Biological Chemistry 250, 6320–6327.CrossRefGoogle ScholarPubMed
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E. & Watanabe, S. (1982). GABA-mediated negative feedback and color opponency in carp retina. Japanese Journal of Physiology 32, 927–935.Google ScholarPubMed
Naka, K.-I. & Ohtsuka, T. (1975). Morphological and functional identifications of catfish retinal neurons. Journal of Neurophysiology 38, 72–91.Google Scholar
Nakatani, K. & Yau, K.-W. (1988 a). Calcium and magnesium fluxes across the plasma membrane of the toad rod outer segment. Journal of Physiology 395, 695–729.Google Scholar
Nakatani, K. & Yau, K.-W. (1988 b). Calcium and light adaptation in retinal rods and cones. Nature (London) 334, 69–71.Google Scholar
Negishi, K., Teranishi, T. & Kato, S. (1984). Opposite effects of ammonia and carbon dioxide on dye coupling between horizontal cells in the carp retina. Brain Research 342, 330–339.Google Scholar
Noma, A. & Tsuboi, N. (1987). Dependence of junctional conductance on proton, calcium and magnesium ions in cardiac paired cells of guinea pig. Journal of Physiology 382, 193–211.Google Scholar
Oakley, B. & Wen, R. (1989). Extracellular pH in the isolated retina of the toad in darkness and during illumination. Journal of Physiology 419, 353–378.CrossRefGoogle ScholarPubMed
Perlman, I., Normann, R.A., Chandler, J.P. & Lipetz, L.E. (1990). Effects of calcium ions on L-type horizontal cells in the isolated turtle retina. Visual Neuroscience 4, 53–62.CrossRefGoogle ScholarPubMed
Pickford, J. (1969). Analysis of Water Surge. New York: Gordon and Breach Science Publishers.Google Scholar
Rowe, J.S. (1987). Effects of external calcium on horizontal cells in the superfused goldfish retina. Neuroscience Research (Suppl.) 6, S147–S164.Google Scholar
Rowe, J.S. & Ruddock, K.H. (1982). Depolarization of retinal horizontal cells by excitatory amino acid neurotransmitter agonists. Neuroscience Letters 30, 257–262.CrossRefGoogle ScholarPubMed
Schnetkamp, P.P.M. (1986). Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. Journal of Physiology 373, 25–45.Google Scholar
Spray, D.C., Harris, A.L. & Bennett, M.V.L. (1981). Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 211, 712–715.Google Scholar
Toyoda, J., Hashimoto, H. & Ohtsu, K. (1973). Bipolar-amacrine transmission in the carp retina. Vision Research 13, 295–307.CrossRefGoogle ScholarPubMed
Winkler, B.S. (1981). Glycolytic and oxidative metabolism in relation to retinal function. Journal of General Physiology 77, 667–692.CrossRefGoogle ScholarPubMed
Yang, X.L., Tauchi, M. & Kaneko, A. (1982). Quantitative analysis of photoreceptor inputs to external horizontal cells of the goldfish retina. Japanese Journal of Physiology 32, 399–420.Google ScholarPubMed
Yau, K.-W. & Nakatani, K. (1984). Cation selectivity of light-sensitive conductance in retinal rods. Nature 309, 352–354.CrossRefGoogle ScholarPubMed
Yau, K.-W. & Nakatani, K. (1985). Light-induced reduction of cyto-plasmic free calcium in retinal rod outer segment. Nature (London) 313, 579–582.CrossRefGoogle Scholar
Yau, K.-W. & Nakatani, K. (1988). Sodium-dependent calcium efflux at the outer segment of the retinal cone. Biophysical Journal 53, 473a.Google Scholar
Yoshikami, S., George, J.S. & Hagins, W.A. (1980). Light-induced Ca fluxes from outer segment layer of vertebrate retinas. Nature (London) 286, 395–398.CrossRefGoogle Scholar