Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-18T06:05:45.983Z Has data issue: false hasContentIssue false
  • English
  • Français

Calcium gradients and light-evoked calcium changes outside rods in the intact cat retina

Published online by Cambridge University Press:  02 June 2009

Ron P. Gallemore ,
Jian-Dong Li ,
Victor I. Govardovskii  and
Roy H. Steinberg
Ron P. Gallemore
Affiliation:
Departments of Physiology and Ophthalmology, University of California, San Francisco
Jian-Dong Li
Affiliation:
Departments of Physiology and Ophthalmology, University of California, San Francisco
Victor I. Govardovskii
Affiliation:
Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, Russia
Roy H. Steinberg
Affiliation:
Departments of Physiology and Ophthalmology, University of California, San Francisco
Get access Rights & Permissions [Opens in a new window]

Abstract

We have studied light-evoked changes in extracellular Ca2+ concentration in the intact cat eye using ion-sensitive double-barreled microelectrodes. Two prominent changes in Ca2+ concentration were observed that differed in retinal location. There was a light-evoked increase in accompanied by brief ON and OFF transients, which was maximal in the inner plexiform layer and was not further studied. There was an unexpected sustained light-evoked decrease in of relatively rapid onset and offset, which was maximal in the distalmost region of the subretinal space (SRS). in the SRS was 1.0 mM higher than in the vitreous humor during dark adaptation and this transretinal gradient disappeared during rod-saturating illumination. After correcting for the light-evoked increase in the volume of the SRS, an increase in the total Ca2+ content of the SRS during illumination was revealed, which presumably represents the Ca2+ released by rods. To explain the light-evoked changes, we used the diffusion model described in the accompanying paper (Li et al., 1994b), with the addition of light-dependent sources of Ca2+ at the retina/retinal pigment epithelium (RPE) border and rod outer segments. We conclude that a drop in around photoreceptors, which persists during illumination and reduces a transretinal Ca2+ gradient, is the combined effect of the light-evoked SRS volume increase, Ca2+ release from photoreceptors, and an unidentified mechanism(s), which is presumably Ca2+ transport by the RPE. The relatively rapid onset and offset of the decrease remains unexplained. These steady-state shifts in should have significant effects on photoreceptor function, especially adaptation.

Keywords

CalciumCatPhotoreceptor(s)Subretinal spaceExtracellular volume
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 753 - 761
Copyright
Copyright © Cambridge University Press 1994

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

Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. Journal of Physiology (London) 331, 253–284.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Nunn, B.J. (1986). Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. Journal of Physiology (London) 371, 115–145.Google Scholar
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology (London) 357, 575–607.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology (London) 288, 589–611.Google Scholar
Bito, L.Z. (1970). Intraocular fluid dynamics. I. Steady-state concentration gradients of magnesium, potassium and calcium in relation to the sites and mechanisms of ocular cation transport processes. Experimental Eye Research 10, 102–116.Google Scholar
Cervetto, L., Pasino, E. & Torre, V. (1977). Electrical responses of rods in the retina of Bufo marinus. Journal of Physiology 267, 17–51.Google Scholar
Dick, E. & Miller, R.F. (1985). Extracellular K+ activity changes related to electroretinogram components. I. Amphibian (I-type) retinas. Journal of Physiology 426, 297–316.Google Scholar
Fajn, G.L. & Matthews, H.R. (1990). Calcium and the mechanism of light adaptation in vertebrate photoreceptors. Trends in Neuro-sciences 13, 378–384.Google Scholar
Fain, G.L., Lamb, T.D., Matthews, H.R. & Murphy, R.L.W. (1989). Cytoplasmic calcium concentration as the messenger for light adaptation in salamander rods. Journal of Physiology (London) 416, 215–243.CrossRefGoogle ScholarPubMed
Fain, G.L., Quandt, F.N. & Gerschenfeld, H.M. (1977). Calcium-dependent regenerative responses in rods. Nature (London) 269, 707–710.Google Scholar
Fisher, S.D. & Steinberg, R.H. (1982). Origin and organization of pigment epithelial apical projections to cones in cat retina. Journal of Comparative Neurology 206, 131–145.Google Scholar
Flaming, D.G. & Brown, K.T. (1979). Effect of calcium on the intensity-response curve of toad rods. Nature 278, 852–853.CrossRefGoogle ScholarPubMed
Gallemore, R.P., & Steinberg, R.H. (1989). Effects of DIDS on the chick retinal pigment epithelium. I. Membrane potentials, apparent resistances, and mechanisms. Journal of Neuroscience 9(6), 1968-1976.Google Scholar
Gailemore, R.P., Yamamoto, F. & Steinberg, R.H. (1990). gradients and light-evoked changes in cat retina, in vivo. Society of Neuroscience (Abstract) 16, 714.Google Scholar
Gold, G.H. (1986). Plasma membrane calcium fluxes in intact rods are inconsistent with the “calcium hypothesis ”. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1150–1154.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.CrossRefGoogle ScholarPubMed
Govardovskii, V.J., Berman, A.L., Bykov, K.A. & Skachkov, S.N. (1987). The role of Ca++ and cyclic GMP in excitation and adaptation of vertebrate photoreceptors. In Retinal Proteins: Proceedings of an International Conference, ed. Ovchinnikov, Y.A., pp. 15–31. Utrecht, Netherlands: VNU Science Press.Google Scholar
Govardovskii, V.J., Li, J.-D., Dmitriev, A.V. & Steinberg, R.H. (1994). Mathematical model of TMA+ diffusion and prediction of light-dependent subretinal hydration in chick retina. Investigative Ophthalmology and Visual Science 35 (in press).Google Scholar
Hageman, G.S. & Johnson, L.V. (1991). Structure, composition and function of the retinal interphotoreceptor matrix. In Progress in Retina/Research, Vol. 10, ed. Osborne, N. & Chader, G., pp. 207–291. New York: Pergamon Press.Google Scholar
Hodgkin, A.L. & Nunn, B.J. (1987). The effects of ions on sodium-calcium exchange in salamander rods. Journal Physiology 391, 371–398.Google Scholar
Huang, B. & Karwoski, C. (1992). Light-evoked expansion of sub-retinal space volume in the retina of the frog. Journal of Neuroscience 12(11), 4243–4252.Google Scholar
Koch, K.-W. (1992). Biochemical mechanism of light adaptation in vertebrate photoreceptors. Trends in Biochemical Science 17, 307–311.CrossRefGoogle ScholarPubMed
Koch, K.-W. & Stryer, L. (1988). Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature (London) 334, 64–66.Google Scholar
Lamb, T.D. & Matthews, H.R. (1988). External and internal actions in the response of salamander rods to altered external calcium concentration. Journal of Physiology 403, 473–494.Google Scholar
Li, J.-D., Gallemore, R.P., Dmitriev, A. & Steinberg, R.H. (1994 a). Light-dependent hydration of the space surrounding photoreceptors in chick retina. Investigative Ophthalmology and Visual Science (in press).Google ScholarPubMed
Li, J.-D., Govardovskii, V. & Steinberg, R.H. (1994 b). Light-dependent hydration of the space surrounding photoreceptors in the cat retina. Visual Neuroscience 11, 743–752.Google Scholar
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.Google Scholar
Matthews, H.R., Murphy, R.L.W., Fajn, G.L. & Lamb, T.D. (1988). Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature (London) 334, 67–69.CrossRefGoogle ScholarPubMed
McNaughton, P.A. (1990). Light response of vertebrate photoreceptors. Physiological Reviews 70, 847–883.Google Scholar
McNaughton, P.A., Cervetto, L. & Nunn, B.J. (1986). Measurement of the intracellular free calcium concentration in salamander rods. Nature 322, 261–263.Google Scholar
Miller, D.L. & Korenbrot, J.I. (1987). Kinetics of light-dependent Ca fluxes across the plasma membrane of rod outer segments: a dynamic model of the regulation of cytoplasmic Ca concentration. Journal of General Physiology 90, 397–425.Google Scholar
Miller, S.S. & Steinberg, R.H. (1977). Active transport of ions across frog retinal pigment epithelium. Experimental Eye Research 25, 235–248.Google Scholar
Nakatani, K. & Yau, K.-W. (1988). Calcium and magnesium fluxes across the plasma membrane of the rod outer segment. Journal of Physiology (London) 395, 695–729.Google Scholar
Pugh, E.N. & Lamb, T.D. (1990). Cyclic GMP and calcium: The internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Research 30, 1923–1948.Google Scholar
Ratto, G.M., Payne, R., Owen, W.G. & Tsien, R.Y. (1988). The concentration of cytosolic free Ca2+ in vertebrate rod outer segments measured with fura2. Journal of Neuroscience 8, 3240–3246.CrossRefGoogle ScholarPubMed
Schnetkamp, P.P.M. (1989). Na-Ca or Na-Ca-K exchange in rod photoreceptors. Progress in Biophysics and Molecular Biology 54, 1–29.Google Scholar
Steinberg, R.H. (1969). The rod after-effect in S-potentials from the cat retina. Vision Research 9, 1345–1355.Google Scholar
Steinberg, R.H., Reid, M. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229–248.Google Scholar
Steinberg, R.H. & Wood, I. (1974). Pigment epithelial cell ensheathment of cone outer segments in the retina of the domestic cat. Proceedings of the Royal Society B (London) 187, 461–478.Google Scholar
Uehara, F., Matthes, M.T., Yasumura, D. & la Vail, M.M. (1990). Light-evoked changes in the interphotoreceptor matrix. Science 248, 1633–1636.CrossRefGoogle ScholarPubMed
Yau, K.-W. & Nakatani, K. (1985). Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature (London) 313, 579–582.Google Scholar
Yoshikami, S., George, J.S. & Hagins, W.A. (1980). Light-induced calcium-fluxes from outer segment layer of vertebrate retinas. Nature (London) 286, 395–398.Google Scholar