Abstract
Electroretinogram (ERG) and extracellular potassium activity (K+o) measurements were carried out in isolated superfused rabbit eyecup preparations under control conditions and during the application of pharmacological agents that selectively modify the light-responsive retinal network. Light-evoked K+o changes in the rabbit (E-type) retina resemble those previously described in amphibian (I-type) retinas. Different components of the light-evoked K+o changes can be distinguished on the bases of retinal depth, V vs. log I properties, and their responses to pharmacological agents. We find two separable sources of light-evoked increases in extracellular K+: a proximal source and a distal source. The properties of the distal light-evoked K+o increase are consistent with the hypothesis that it initiates a K+- mediated current through Muller cells that is detected as the primary voltage of the electroretinographic b-wave. These experiments also support previous studies indicating that both the corneal-positive component of c-wave and the corneal-negative slow PIII potential result from K+-mediated influences on, respectively, the retinal pigment epithelium and Muller cells.
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- BROWN K. T., WIESEL T. N. Analysis of the intraretinal electroretinogram in the intact cat eye. J Physiol. 1961 Sep;158:229–256. doi: 10.1113/jphysiol.1961.sp006767. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dick E., Miller R. F. Extracellular K+ activity changes related to electroretinogram components. I. Amphibian (I-type) retinas. J Gen Physiol. 1985 Jun;85(6):885–909. doi: 10.1085/jgp.85.6.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dick E., Miller R. F. Light-evoked potassium activity in mudpuppy retina: its relationship to the b-wave of the electroretinogram. Brain Res. 1978 Oct 13;154(2):388–394. doi: 10.1016/0006-8993(78)90711-4. [DOI] [PubMed] [Google Scholar]
- Granit R. Two types of retinae and their electrical responses to intermittent stimuli in light and dark adaptation. J Physiol. 1935 Dec 16;85(4):421–438. doi: 10.1113/jphysiol.1935.sp003329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henkind P. The retinal vascular system of the domestic cat. Exp Eye Res. 1966 Jan;5(1):10–20. doi: 10.1016/s0014-4835(66)80015-5. [DOI] [PubMed] [Google Scholar]
- Karowski C. J., Proenza L. M. Relationship between Müller cell responses, a local transretinal potential, and potassium flux. J Neurophysiol. 1977 Mar;40(2):244–259. doi: 10.1152/jn.1977.40.2.244. [DOI] [PubMed] [Google Scholar]
- Karwoski C. J., Proenza L. M. Light-evoked changes in extracellular potassium concentration in munpuppy retina. Brain Res. 1978 Mar 10;142(3):515–530. doi: 10.1016/0006-8993(78)90913-7. [DOI] [PubMed] [Google Scholar]
- Karwoski C. J., Proenza L. M. Neurons, potassium, and glia in proximal retina of Necturus. J Gen Physiol. 1980 Feb;75(2):141–162. doi: 10.1085/jgp.75.2.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karwoski J., Criswell M. H., Proenza L. M. Laminar separation of light-evoked K+ flux and field potentials in frog retina. Invest Ophthalmol Vis Sci. 1978 Jul;17(7):678–682. [PubMed] [Google Scholar]
- Kline R. P., Ripps H., Dowling J. E. Generation of b-wave currents in the skate retina. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5727–5731. doi: 10.1073/pnas.75.11.5727. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lurie M., Marmor M. F. Similarities between the c-wave and slow PIII in the rabbit eye. Invest Ophthalmol Vis Sci. 1980 Sep;19(9):1113–1117. [PubMed] [Google Scholar]
- Masland R. H., Ames A., 3rd Responses to acetylcholine of ganglion cells in an isolated mammalian retina. J Neurophysiol. 1976 Nov;39(6):1220–1235. doi: 10.1152/jn.1976.39.6.1220. [DOI] [PubMed] [Google Scholar]
- Masland R. H., Livingstone C. J. Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. J Neurophysiol. 1976 Nov;39(6):1210–1219. doi: 10.1152/jn.1976.39.6.1210. [DOI] [PubMed] [Google Scholar]
- Massey S. C., Neal M. J. The light evoked release of acetylcholine from the rabbit retina iN vivo and its inhibition by gamma-aminobutyric acid. J Neurochem. 1979 Apr;32(4):1327–1329. doi: 10.1111/j.1471-4159.1979.tb11062.x. [DOI] [PubMed] [Google Scholar]
- Massey S. C., Redburn D. A. A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. J Neurosci. 1982 Nov;2(11):1633–1643. doi: 10.1523/JNEUROSCI.02-11-01633.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller R. F., Dowling J. E. Intracellular responses of the Müller (glial) cells of mudpuppy retina: their relation to b-wave of the electroretinogram. J Neurophysiol. 1970 May;33(3):323–341. doi: 10.1152/jn.1970.33.3.323. [DOI] [PubMed] [Google Scholar]
- Miller R. F. Role of K + in generation of b-wave of electroretinogram. J Neurophysiol. 1973 Jan;36(1):28–38. doi: 10.1152/jn.1973.36.1.28. [DOI] [PubMed] [Google Scholar]
- Newman E. A. B-wave currents in the frog retina. Vision Res. 1979;19(3):227–234. doi: 10.1016/0042-6989(79)90167-6. [DOI] [PubMed] [Google Scholar]
- Newman E. A. Current source-density analysis of the b-wave of frog retina. J Neurophysiol. 1980 May;43(5):1355–1366. doi: 10.1152/jn.1980.43.5.1355. [DOI] [PubMed] [Google Scholar]
- Newman E. A., Odette L. L. Model of electroretinogram b-wave generation: a test of the K+ hypothesis. J Neurophysiol. 1984 Jan;51(1):164–182. doi: 10.1152/jn.1984.51.1.164. [DOI] [PubMed] [Google Scholar]
- Oakley B., 2nd, Green D. G. Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol. 1976 Sep;39(5):1117–1133. doi: 10.1152/jn.1976.39.5.1117. [DOI] [PubMed] [Google Scholar]
- Oakley B., 2nd Potassium and the photoreceptor-dependent pigment epithelial hyperpolarization. J Gen Physiol. 1977 Oct;70(4):405–425. doi: 10.1085/jgp.70.4.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen J. S., Miller R. F. Spontaneous slow potentials and spreading depression in amphibian retina. J Neurophysiol. 1977 Jul;40(4):752–767. doi: 10.1152/jn.1977.40.4.752. [DOI] [PubMed] [Google Scholar]
- Rager G. The cellular origin of the b-wave in the electroretinogram -- a developmental approach. J Comp Neurol. 1979 Nov 15;188(2):225–244. doi: 10.1002/cne.901880203. [DOI] [PubMed] [Google Scholar]
- Schmidt R., Steinberg R. H. Rod-dependent intracellular responses to light recorded from the pigment epithelium of the cat retina. J Physiol. 1971 Aug;217(1):71–91. doi: 10.1113/jphysiol.1971.sp009560. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimazaki H., Karwoski C. J., Proenza L. M. Aspartate-induced dissociation of proximal from distal retinal activity in the mudpuppy. Vision Res. 1984;24(6):587–595. doi: 10.1016/0042-6989(84)90113-5. [DOI] [PubMed] [Google Scholar]
- Steinberg R. H. Incremental responses to light recorded from pigment epithelial cells and horizontal cells of the cat retina. J Physiol. 1971 Aug;217(1):93–110. doi: 10.1113/jphysiol.1971.sp009561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steinberg R. H., Miller S. Aspects of electrolyte transport in frog pigment epithelium. Exp Eye Res. 1973 Aug 24;16(5):365–372. doi: 10.1016/0014-4835(73)90130-9. [DOI] [PubMed] [Google Scholar]
- Steinberg R. H., Oakley B., 2nd, Niemeyer G. Light-evoked changes in [K+]0 in retina of intact cat eye. J Neurophysiol. 1980 Nov;44(5):897–921. doi: 10.1152/jn.1980.44.5.897. [DOI] [PubMed] [Google Scholar]
- Steinberg R. H., Schmidt R., Brown K. T. Intracellular responses to light from cat pigment epithelium: origin of the electroretinogram c-wave. Nature. 1970 Aug 15;227(5259):728–730. doi: 10.1038/227728a0. [DOI] [PubMed] [Google Scholar]
- Tomita T. Electrophysiological studies of retinal cell function. Invest Ophthalmol. 1976 Mar;15(3):171–187. [PubMed] [Google Scholar]
- Welinder E., Textorius O., Nilsson S. E. Effects of intravitreally injected DL-alpha-aminoadipic acid on the c-wave of the D.C.-recorded electroretinogram in albino rabbits. Invest Ophthalmol Vis Sci. 1982 Aug;23(2):240–245. [PubMed] [Google Scholar]
- Witkovsky P., Dudek F. E., Ripps H. Slow PIII component of the carp electroretinogram. J Gen Physiol. 1975 Feb;65(2):119–134. doi: 10.1085/jgp.65.2.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yanagida T., Tomita T. Local potassium concentration changes in the retina and the electroretinographic (ERG) b-wave. Brain Res. 1982 Apr 15;237(2):479–483. doi: 10.1016/0006-8993(82)90459-0. [DOI] [PubMed] [Google Scholar]
- Zuckerman R. Ionic analysis of photoreceptor membrane currents. J Physiol. 1973 Dec;235(2):333–354. doi: 10.1113/jphysiol.1973.sp010390. [DOI] [PMC free article] [PubMed] [Google Scholar]