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The origin of slow PIII in frog retina: Current source density analysis in the eyecup and isolated retina

Published online by Cambridge University Press:  02 June 2009

Xijing Xu
Affiliation:
Vision Research Laboratory, Department of Psychology, University of Georgia, Athens
Chester J. Karwoski
Affiliation:
Vision Research Laboratory, Department of Psychology, University of Georgia, Athens

Abstract

The objective of this research was to determine the sources and sinks of current underlying the slow PIII component of the electroretinogram. Current source density analysis of the ERG evoked by diffuse light flashes was performed in eyecup and isolated retinas of frog. Blockade of synaptic transmission with aminophosphonobutyric + kynurenic acids simplified the CSD profiles through the retina. In addition to the photoreceptor source/sink pair, there was evidence for a major slow PIII source near the outer limiting membrane, a major sink near the inner limiting membrane, and a small source near the inner plexiform layer. Addition of Ba2+ abolished the slow PIII source/sinks, and it left only the photoreceptor source and sink. The results support the idea that slow PIII originates through K+ spatial buffering by Müller cells. Specifically, the light-evoked decrease in [K+]0 in the subretinal space causes a primary K+ efflux from Müller cells (current source) and a primary K+ influx at the Müller cell endfeet (current sink). A decrease in [K+]0 in the proximal retina, caused by diffusion of K+ to the subretinal space, results in K+ efflux (the current source) at the inner plexiform layer.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

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References

Arden, G.B. (1976). Voltage gradients across the receptor layer of the isolated rat retina. Journal of Physiology 256, 333360.CrossRefGoogle ScholarPubMed
Bolnick, D.A., Walter, A.E. & Sillamn, A.J. (1979). Barium suppresses slow PIII in perfused bullfrog retina. Vision Research 19, 11171120.CrossRefGoogle ScholarPubMed
Brown, K.T., Flaming, D.C. (1978). Opposing effects of calcium and barium in vertebrate rod photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 75, 15871590.CrossRefGoogle ScholarPubMed
Faber, D. (1969). Analysis of the slow transretinal potentials in response to light. Ph.D. Thesis, University of New York (Buffalo).Google Scholar
Fain, G.L., Gerschenfeld, J.M. & Quandt, F.N. (1980). Calcium spikes in toad rods. Journal of Physiology 303, 495613.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Steinberg, R.H. (1990). Origin of negative potentials in the light-adapted ERG of cat retina. Journal of Neurophysiology 63, 13331346.CrossRefGoogle ScholarPubMed
Fujimoto, M. & Tomita, T. (1981). Field potentials induced by injection of potassium ion into frog retina: A test of current interpretations of the electroretinographic (ERG) b-wave. Brain Research 204, 5164.CrossRefGoogle ScholarPubMed
Griff, E.R. (1991). Electroretinographic components arising in the distal retina. In Principles and Practice of Clinical Electrophysiology of Vision, ed. Heckenlively, J.R. & Arden, G.B., pp. 9198. St. Louis, Missouri: Mosby Year Book.Google Scholar
Hagins, W.A., Penn, R.D. & Yoshikami, S. (1970). Dark current and photocurrent in retinal rods. Biophysics Journal 10, 380412.CrossRefGoogle ScholarPubMed
Kapousta-Bruneau, N., Green, D.G. & Liu, S.B. (1996). Do Müller cells have a role in generating the b-wave of the ERG? Investigative Ophthalmology and Visual Science 37, S348.Google Scholar
Karwoski, C.J. (1991). Introduction to the origins of electroretinographic components. In Principles and Practice of Clinical Electrophysiology of Vision, ed. Heckenlively, J.R. & Arden, G.B., pp. 8790. St. Louis, Missouri: Mosby Year Book.Google Scholar
Karwoski, C.J., Frambach, D.A. & Proenza, L.M. (1985). Laminar profile of resistivity in frog retina. Journal of Neurophysiology 54, 16071619.CrossRefGoogle ScholarPubMed
Karwoski, C.J., Xu, X. & Yu, H. (1996). Current-source density analysis of the electroretinogram of the frog: Methodological issues and origin of components. Journal of the Optical Society of America A 13, 549556.CrossRefGoogle ScholarPubMed
Newman, E.A. (1994). Müller cells and the retinal pigment epithelium. In Principles and Practice of Ophthalmology, ed. Albert, D.M. & Jakobiec, F.A., pp. 398419. Philadelphia, Pennsylvania: W.B. Saunders Co.Google Scholar
Newman, E.A., Frambach, D.A. & Odette, L.L. (1984). Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225, 11741175.CrossRefGoogle ScholarPubMed
Noell, W.K. (1953). Studies on the electrophysiology and the metabolism of the retina. USAF SAM Project No. 21–2101–004, Randolph Field, TX, pp. 1122.Google Scholar
Oakley, B., Flaming, D.G. & Brown, K.T. (1979). Effects of the rod receptor potential upon retinal extracellular potassium concentration. Journal of General Physiology 74, 713737.CrossRefGoogle ScholarPubMed
Oakley, B., Katz, B.J., Xu, Z. & Zheng, J. (1992). Spatial buffering of extracellular potassium by Müller (glial) cells in the toad retina. Experimental Eye Research 55, 539550.CrossRefGoogle Scholar
Orkand, R.K. (1987). Glial-interstitial fluid exchange. Annals of the New York Academy of Sciences 481, 269272.CrossRefGoogle Scholar
Orkand, R.K., Nicholls, J.G. & Kuffler, S.W. (1966). Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amhphibia. Journal of Neurophysiology 39, 788806.CrossRefGoogle Scholar
Steinberg, R.H., Frishman, L.J. & Sieving, P.A. (1991). Negative components of the electroretinogram from proximal retina and photoreceptor. In Progress in Retinal Research, 10, ed. Osborne, N.N. & Chader, G.J., pp. 121160. Oxford: Pergamon Press.Google Scholar
Steinberg, R.H., Linsenmeier, R.A. & Griff, E.R. (1985). Retinal pigment epithelial cell contributions to the electroretinogram and electro-oculogram. In Progress in Retinal Research, 4, ed. Osborne, N.N. & Chader, G.J., pp. 3366. Oxford: Pergamon Press.Google Scholar
Steinberg, R.H., Oakley, B. & Niemeyer, G. (1980). Light-evoked changes in [K+] in retina of intact cat eye. Journal of Neurophysiology 44, 897921.CrossRefGoogle ScholarPubMed
Stockton, R.A. & Slaughter, M.M. (1989). The b-wave of the electroretinogram: A reflection of ON bipolar cell activity. Journal of General Physiology 93, 101122.CrossRefGoogle ScholarPubMed
Wakabayashi, K., Gieser, J. & Sieving, P.A. (1988). Aspartate separation of the scotopic threshold response (STR) from the photoreceptor a-wave of the cat and monkey ERG.RG. Investigative Ophthalmology and Visual Science 29, 16151622.Google Scholar
Wen, R. & Oakley, B. (1990). K+-evoked Müller cell depolarization generates b-wave of the electroretinogram in toad retina. Proceedings of the National Academy of Sciences of the U.S.A. 87, 21172121.CrossRefGoogle ScholarPubMed
Xu, X. & Karwoski, C.J. (1994 a). Current source density (CSD) analysis of retinal field potentials. I. Methodological considerations and depth profiles. Journal of Neurophysiology 72, 8495.CrossRefGoogle ScholarPubMed
Xu, X. & Karwoski, C.J. (1994 b). Current source density (CSD) analysis of retinal field potentials. II. Pharmacological analysis of the b-wave and M-wave. Journal of Neurophysiology 72, 96105.CrossRefGoogle Scholar
Xu, X. & Karwoski, C.J. (1995). Current source density analysis of the electroretinographic d-wave. Journal of Neurophysiology 73, 24592469.CrossRefGoogle ScholarPubMed
Xu, X. & Karwoski, C.J. (1996). Rabbit ERG: Current source density (CSD) analysis. Investigative Ophthalmology and Visual Science 37, SI36.Google Scholar
Xu, X., Xu, J., Huang, B., Livsey, C.T. & Karwoski, C.J. (1991). Comparison of pharmacological agents (aspartate vs. aminophosphonobu-tyric plus kynurenic acids) to block synaptic transmission from retinal photoreceptors in frog. Experimental Eye Research 52, 691698.CrossRefGoogle ScholarPubMed
Zuckerman, R. (1973). Ionic analysis of photoreceptor membrane currents. Journal of Physiology 235, 333354.CrossRefGoogle ScholarPubMed