Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1985 Jun 1;85(6):885–909. doi: 10.1085/jgp.85.6.885

Extracellular K+ activity changes related to electroretinogram components. I. Amphibian (I-type) retinas

PMCID: PMC2215781  PMID: 3926945

Abstract

Electroretinographic (ERG) and extracellular potassium activity measurements were carried out in superfused eyecup preparations of several amphibians. Light-evoked changes in extracellular K+ activity were characterized on the bases of depth profile analysis and latency measurements and through the application of pharmacological agents that have selective actions on the retinal network. Three different extracellular potassium modulations evoked at light onset were identified and characterized according to their phenomenological and pharmacological properties. These modulations include two separable sources of light-evoked increases in extracellular K+: (a) a proximal source that is largely post-bipolar in origin, and (b) a distal source that is primarily or exclusively of depolarizing bipolar cell origin. The pharmacological properties of the distal extracellular potassium increase closely parallel those of the b-wave. A distal light-evoked decrease in extracellular potassium appears to be associated with the slow PIII potential, based on a combination of simultaneous intracellular Muller cell recordings and extracellular ERG and potassium activity measurements before and during pharmacological isolation of the photoreceptor responses. The extracellular potassium activity increases are discussed with respect to the Muller cell theory of b-wave generation.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BRINDLEY G. S., HAMASAKI D. I. The properties and nature of the R membrane of the frog's eye. J Physiol. 1963 Jul;167:599–606. doi: 10.1113/jphysiol.1963.sp007170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berger S. J., McDaniel M. L., Carter J. G., Lowry O. H. Distribution of four potential transmitter amino acids in monkey retina. J Neurochem. 1977 Jan;28(1):159–163. doi: 10.1111/j.1471-4159.1977.tb07721.x. [DOI] [PubMed] [Google Scholar]
  3. Bonaventure N., Roussel G., Wioland N. Effects of DL-alpha-amino adipic acid on Müller cells in frog and chicken retinae in vivo: relation to ERG b wave, ganglion cell discharge and tectal evoked potentials. Neurosci Lett. 1981 Nov 18;27(1):81–87. doi: 10.1016/0304-3940(81)90209-3. [DOI] [PubMed] [Google Scholar]
  4. Caldwell J. H., Daw N. W., Wyatt H. J. Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J Physiol. 1978 Mar;276:277–298. doi: 10.1113/jphysiol.1978.sp012233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cervetto L., Piccolino M. Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science. 1974 Feb 1;183(4123):417–419. doi: 10.1126/science.183.4123.417. [DOI] [PubMed] [Google Scholar]
  6. Coles J. A., Tsacopoulos M. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol. 1979 May;290(2):525–549. doi: 10.1113/jphysiol.1979.sp012788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dacheux R. F., Frumkes T. E., Miller R. F. Pathways and polarities of synaptic interactions in the inner retina of the mudpuppy: I. Synaptic blocking studies. Brain Res. 1979 Jan 26;161(1):1–12. doi: 10.1016/0006-8993(79)90191-4. [DOI] [PubMed] [Google Scholar]
  8. Dacheux R. F., Miller R. F. Photoreceptor-bipolar cell transmission in the perfused retina eyecup of the mudpuppy. Science. 1976 Mar 5;191(4230):963–964. doi: 10.1126/science.175443. [DOI] [PubMed] [Google Scholar]
  9. Dick E., Miller R. F., Bloomfield S. Extracellular K+ activity changes related to electroretinogram components. II. Rabbit (E-type) retinas. J Gen Physiol. 1985 Jun;85(6):911–931. doi: 10.1085/jgp.85.6.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dowling J. E., Ripps H. Potassium and retinal sensitivity. Brain Res. 1976 May 14;107(3):617–622. doi: 10.1016/0006-8993(76)90149-9. [DOI] [PubMed] [Google Scholar]
  11. FRANK K., FUORTES M. G., NELSON P. G. Voltage clamp of motoneuron soma. Science. 1959 Jul 3;130(3366):38–39. doi: 10.1126/science.130.3366.38. [DOI] [PubMed] [Google Scholar]
  12. Gardner-Medwin A. R. A study of the mechanisms by which potassium moves through brain tissue in the rat. J Physiol. 1983 Feb;335:353–374. doi: 10.1113/jphysiol.1983.sp014539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Hagins W. A., Penn R. D., Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970 May;10(5):380–412. doi: 10.1016/S0006-3495(70)86308-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. Kennedy A. J., Neal M. J., Lolley R. N. The distribution of amino acids within the rat retina. J Neurochem. 1977 Jul;29(1):157–159. doi: 10.1111/j.1471-4159.1977.tb03938.x. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Lam D. M., Steinman L. The uptake of ( - 3 H) aminobutyric acid in the goldfish retina. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2777–2781. doi: 10.1073/pnas.68.11.2777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lam D. M. Synaptic chemistry of identified cells in the vertebrate retina. Cold Spring Harb Symp Quant Biol. 1976;40:571–579. doi: 10.1101/sqb.1976.040.01.053. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Matsuura T., Miller W. H., Tomita T. Cone-specific c-wave in the turtle retina. Vision Res. 1978;18(7):767–775. doi: 10.1016/0042-6989(78)90115-3. [DOI] [PubMed] [Google Scholar]
  25. Miller R. F., Dacheux R. F., Frumkes T. E. Amacrine cells in Necturus retina: evidence for independent gamma-aminobutyric acid- and glycine-releasing neurons. Science. 1977 Nov 18;198(4318):748–750. doi: 10.1126/science.910159. [DOI] [PubMed] [Google Scholar]
  26. Miller R. F., Dacheux R. F. Synaptic organization and ionic basis of on and off channels in mudpuppy retina. I. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolar cells, and amacrine cells. J Gen Physiol. 1976 Jun;67(6):639–659. doi: 10.1085/jgp.67.6.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Miller R. F., Frumkes T. E., Slaughter M., Dacheux R. F. Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. I. Receptors, horizontal cells, bipolars, and G-cells. J Neurophysiol. 1981 Apr;45(4):743–763. doi: 10.1152/jn.1981.45.4.743. [DOI] [PubMed] [Google Scholar]
  29. Miller R. F., Frumkes T. E., Slaughter M., Dacheux R. F. Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. II. Amacrine and ganglion cells. J Neurophysiol. 1981 Apr;45(4):764–782. doi: 10.1152/jn.1981.45.4.764. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. NOELL W. K. The effect of iodoacetate on the vertebrate retina. J Cell Physiol. 1951 Apr;37(2):283–307. doi: 10.1002/jcp.1030370209. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Newman E. A., Frambach D. A., Odette L. L. Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science. 1984 Sep 14;225(4667):1174–1175. doi: 10.1126/science.6474173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Newman E. A. Regional specialization of retinal glial cell membrane. Nature. 1984 May 10;309(5964):155–157. doi: 10.1038/309155a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Niemeyer G. The function of the retina in the perfused eye. Doc Ophthalmol. 1975 Nov 21;39(1):53–116. doi: 10.1007/BF00578759. [DOI] [PubMed] [Google Scholar]
  38. Oakley B., 2nd, Flaming D. G., Brown K. T. Effects of the rod receptor potential upon retinal extracellular potassium concentration. J Gen Physiol. 1979 Dec;74(6):713–737. doi: 10.1085/jgp.74.6.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. 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]
  41. Penn R. D., Hagins W. A. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature. 1969 Jul 12;223(5202):201–204. doi: 10.1038/223201a0. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. 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]
  44. 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]
  45. Somjen G. G. Extracellular potassium in the mammalian central nervous system. Annu Rev Physiol. 1979;41:159–177. doi: 10.1146/annurev.ph.41.030179.001111. [DOI] [PubMed] [Google Scholar]
  46. Starr M. S., Voaden M. J. The uptake of ( 14 C) -aminobutyric acid by the isolated retina of the rat. Vision Res. 1972 Apr;12(4):549–557. doi: 10.1016/0042-6989(72)90150-2. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. 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]
  50. 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]
  51. Straschill M., Perwein J. The inhibition of retinal ganglion cells by catecholeamines and gamma-aminobutyric acid. Pflugers Arch. 1969;312(3):45–54. doi: 10.1007/BF00588530. [DOI] [PubMed] [Google Scholar]
  52. Szamier R. B., Ripps H., Chappell R. L. Changes in ERG b-wave and Müller cell structure induced by alpha-aminoadipic acid. Neurosci Lett. 1981 Feb 6;21(3):307–312. doi: 10.1016/0304-3940(81)90222-6. [DOI] [PubMed] [Google Scholar]
  53. Tigges J., Brooks B. A., Klee M. R. ERG recordings of a primate pure cone retina (Tupaia glis). Vision Res. 1967 Jul;7(7):553–563. doi: 10.1016/0042-6989(67)90064-8. [DOI] [PubMed] [Google Scholar]
  54. Tomita T. Electrophysiological studies of retinal cell function. Invest Ophthalmol. 1976 Mar;15(3):171–187. [PubMed] [Google Scholar]
  55. Tomita T., Kaneko A. An intracellular coaxial microelectrode--its construction and application. Med Electron Biol Eng. 1965 Oct;3(4):367–376. doi: 10.1007/BF02476131. [DOI] [PubMed] [Google Scholar]
  56. 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]
  57. 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]
  58. 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]
  59. 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]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES