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. 1984 Sep 1;84(3):475–504. doi: 10.1085/jgp.84.3.475

Reaccumulation of [K+]o in the toad retina during maintained illumination

PMCID: PMC2228745  PMID: 6090581

Abstract

Using K+-selective microelectrodes, [K+]o was measured in the subretinal space of the isolated retina of the toad, Bufo marinus. During maintained illumination, [K+]o fell to a minimum and then recovered to a steady level that was approximately 0.1 mM below its dark level. Spatial buffering of [K+]o by Muller (glial) cells could contribute to this reaccumulation of K+. However, superfusion with substances that might be expected to block glial transport of K+ had no significant effect upon the reaccumulation of K+. These substances included blockers of gK (TEA+, Cs+, Rb+, 4-AP) and a gliotoxin (alpha AAA). Progressive slowing of the rods' Na+/K+ pump (perhaps caused by a light-evoked decrease in [Na+]i) also could contribute to this reaccumulation of K+ by reducing the uptake of K+ from the subretinal space. As evidence for a major contribution by this mechanism, treatments designed to prevent such slowing of the pump reversibly blocked reaccumulation. These treatments included superfusion with 2 microM ouabain, or lowering [K+]o, PO2, or temperature. It is likely that such treatments inhibit the pump, increase [Na+]i, and attenuate any light-evoked decrease in [Na+]i. The results are consistent with the following hypothesis. At light onset, the decrease in rod gNa will reduce the Na+ influx and the resulting rod hyperpolarization will reduce the K+ efflux. In combination with these reduced passive fluxes, the continuing active fluxes will lower both [K+]o and [Na+]i, which in turn will inhibit the pump. In support of this hypothesis, the solutions to a pair of coupled differential equations that model changes in both [K+]o and [Na+]i match quantitatively the time course of the observed changes in [K+]o during and after maintained illumination for all stimuli examined.

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Selected References

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  1. Ballanyi K., Grafe P., ten Bruggencate G. Intracellular free sodium and potassium, post-carbachol hyperpolarization, and extracellular potassium-undershoot in rat sympathetic neurones. Neurosci Lett. 1983 Aug 8;38(3):275–279. doi: 10.1016/0304-3940(83)90381-6. [DOI] [PubMed] [Google Scholar]
  2. Benninger C., Kadis J., Prince D. A. Extracellular calcium and potassium changes in hippocampal slices. Brain Res. 1980 Apr 7;187(1):165–182. doi: 10.1016/0006-8993(80)90502-8. [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. Brown K. T., Flaming D. G. Technique for precision beveling of relatively large micropipettes. J Neurosci Methods. 1979 Mar;1(1):25–34. doi: 10.1016/0165-0270(79)90004-9. [DOI] [PubMed] [Google Scholar]
  5. Chapman R. A., Coray A., McGuigan J. A. Sodium/calcium exchange in mammalian ventricular muscle: a study with sodium-sensitive micro-electrodes. J Physiol. 1983 Oct;343:253–276. doi: 10.1113/jphysiol.1983.sp014891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cohen C. J., Fozzard H. A., Sheu S. S. Increase in intracellular sodium ion activity during stimulation in mammalian cardiac muscle. Circ Res. 1982 May;50(5):651–662. doi: 10.1161/01.res.50.5.651. [DOI] [PubMed] [Google Scholar]
  7. Coles J. A., Orkand R. K. Modification of potassium movement through the retina of the drone (Apis mellifera male) by glial uptake. J Physiol. 1983 Jul;340:157–174. doi: 10.1113/jphysiol.1983.sp014756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Connors B. W., Ransom B. R., Kunis D. M., Gutnick M. J. Activity-dependent K+ accumulation in the developing rat optic nerve. Science. 1982 Jun 18;216(4552):1341–1343. doi: 10.1126/science.7079771. [DOI] [PubMed] [Google Scholar]
  10. Dietzel I., Heinemann U., Hofmeier G., Lux H. D. Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res. 1980;40(4):432–439. doi: 10.1007/BF00236151. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Edwards C. The selectivity of ion channels in nerve and muscle. Neuroscience. 1982 Jun;7(6):1335–1366. doi: 10.1016/0306-4522(82)90249-4. [DOI] [PubMed] [Google Scholar]
  13. Eisner D. A., Lederer W. J. Characterization of the electrogenic sodium pump in cardiac Purkinje fibres. J Physiol. 1980 Jun;303:441–474. doi: 10.1113/jphysiol.1980.sp013298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ellory J. C., Flatman P. W., Stewart G. W. Inhibition of human red cell sodium and potassium transport by divalent cations. J Physiol. 1983 Jul;340:1–17. doi: 10.1113/jphysiol.1983.sp014746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fain G. L., Quandt F. N. The effects of tetraethylammonium and cobalt ions on responses to extrinsic current in toad rods. J Physiol. 1980 Jun;303:515–533. doi: 10.1113/jphysiol.1980.sp013301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Frank R. N., Goldsmith T. H. Effects of cardiac glycosides on electrical activity in the isolated retina of the frog. J Gen Physiol. 1967 Jul;50(6):1585–1606. doi: 10.1085/jgp.50.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fujimoto M., Tomita T. Reconstruction of the slow PIII from the rod potential. Invest Ophthalmol Vis Sci. 1979 Oct;18(10):1091–1093. [PubMed] [Google Scholar]
  18. Gadsby D. C. Activation of electrogenic Na+/K+ exchange by extracellular K+ in canine cardiac Purkinje fibers. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4035–4039. doi: 10.1073/pnas.77.7.4035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Galvan M., Bruggencate G. T., Senekowitsch R. The effects of neuronal stimulation and ouabain upon extracellular K+ and Ca2+ levels in rat isolated sympathetic ganglia. Brain Res. 1979 Jan 19;160(3):544–548. doi: 10.1016/0006-8993(79)91084-9. [DOI] [PubMed] [Google Scholar]
  20. Garay R. P., Garrahan P. J. The interaction of sodium and potassium with the sodium pump in red cells. J Physiol. 1973 Jun;231(2):297–325. doi: 10.1113/jphysiol.1973.sp010234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Gardner-Medwin A. R., Coles J. A., Tsacopoulos M. Clearance of extracellular potassium: evidence for spatial buffering by glial cells in the retina of the drone. Brain Res. 1981 Mar 30;209(2):452–457. doi: 10.1016/0006-8993(81)90169-4. [DOI] [PubMed] [Google Scholar]
  23. Gardner-Medwin A. R., Nicholson C. Changes of extracellular potassium activity induced by electric current through brain tissue in the rat. J Physiol. 1983 Feb;335:375–392. doi: 10.1113/jphysiol.1983.sp014540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Glitsch H. G. Activation of the electrogenic sodium pump in guinea-pig auricles by internal sodium ions. J Physiol. 1972 Feb;220(3):565–582. doi: 10.1113/jphysiol.1972.sp009723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Glynn I. M., Karlish S. J. The sodium pump. Annu Rev Physiol. 1975;37:13–55. doi: 10.1146/annurev.ph.37.030175.000305. [DOI] [PubMed] [Google Scholar]
  26. Griff E. R., Steinberg R. H. Changes in apical [K+] produce delayed basal membrane responses of the retinal pigment epithelium in the gecko. J Gen Physiol. 1984 Feb;83(2):193–211. doi: 10.1085/jgp.83.2.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Hagiwara S., Miyazaki S., Rosenthal N. P. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J Gen Physiol. 1976 Jun;67(6):621–638. doi: 10.1085/jgp.67.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hagiwara S., Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18(1):61–80. doi: 10.1007/BF01870103. [DOI] [PubMed] [Google Scholar]
  30. Heinemann U., Lux H. D. Ceiling of stimulus induced rises in extracellular potassium concentration in the cerebral cortex of cat. Brain Res. 1977 Jan 21;120(2):231–249. doi: 10.1016/0006-8993(77)90903-9. [DOI] [PubMed] [Google Scholar]
  31. Heinemann U., Lux H. D. Undershoots following stimulus-induced rises of extracellular potassium concentration in cerebral cortex of cat. Brain Res. 1975 Jul 25;93(1):63–76. doi: 10.1016/0006-8993(75)90286-3. [DOI] [PubMed] [Google Scholar]
  32. Hille B. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J Gen Physiol. 1967 May;50(5):1287–1302. doi: 10.1085/jgp.50.5.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Kimble E. A., Svoboda R. A., Ostroy S. E. Oxygen consumption and ATP changes of the vertebrate photoreceptor. Exp Eye Res. 1980 Sep;31(3):271–288. doi: 10.1016/s0014-4835(80)80037-6. [DOI] [PubMed] [Google Scholar]
  35. Kline R. P., Kupersmith J. Effects of extracellular potassium accumulation and sodium pump activation on automatic canine Purkinje fibres. J Physiol. 1982 Mar;324:507–533. doi: 10.1113/jphysiol.1982.sp014127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Kunze D. L. Rate-dependent changes in extracellular potassium in the rabbit atrium. Circ Res. 1977 Jul;41(1):122–127. doi: 10.1161/01.res.41.1.122. [DOI] [PubMed] [Google Scholar]
  38. Martin G., Morad M. Activity-induced potassium accumulation and its uptake in frog ventricular muscle. J Physiol. 1982 Jul;328:205–227. doi: 10.1113/jphysiol.1982.sp014260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Meves H., Pichon Y. The effect of internal and external 4-aminopyridine on the potassium currents in intracellularly perfused squid giant axons. J Physiol. 1977 Jun;268(2):511–532. doi: 10.1113/jphysiol.1977.sp011869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Miller S. S., Steinberg R. H. Passive ionic properties of frog retinal pigment epithelium. J Membr Biol. 1977 Sep 15;36(4):337–372. doi: 10.1007/BF01868158. [DOI] [PubMed] [Google Scholar]
  42. Miller S. S., Steinberg R. H. Potassium modulation of taurine transport across the frog retinal pigment epithelium. J Gen Physiol. 1979 Aug;74(2):237–259. doi: 10.1085/jgp.74.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Narahashi T. Chemicals as tools in the study of excitable membranes. Physiol Rev. 1974 Oct;54(4):813–889. doi: 10.1152/physrev.1974.54.4.813. [DOI] [PubMed] [Google Scholar]
  44. Neher E., Lux H. D. Rapid changes of potassium concentration at the outer surface of exposed single neurons during membrane current flow. J Gen Physiol. 1973 Mar;61(3):385–399. doi: 10.1085/jgp.61.3.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nelson M. T., Blaustein M. P. Properties of sodium pumps in internally perfused barnacle muscle fibers. J Gen Physiol. 1980 Feb;75(2):183–206. doi: 10.1085/jgp.75.2.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Nicholson C., ten Bruggencate G., Stöckle H., Steinberg R. Calcium and potassium changes in extracellular microenvironment of cat cerebellar cortex. J Neurophysiol. 1978 Jul;41(4):1026–1039. doi: 10.1152/jn.1978.41.4.1026. [DOI] [PubMed] [Google Scholar]
  47. Oakley B., 2nd Effects of maintained illumination upon [K+]0 in the subretinal space of the isolated retina of the toad. Vision Res. 1983;23(11):1325–1337. doi: 10.1016/0042-6989(83)90108-6. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. 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]
  50. Oakley B., 2nd, Steinberg R. H. Effects of maintained illumination upon [K+]0 in the subretinal space of the frog retina. Vision Res. 1982;22(7):767–773. doi: 10.1016/0042-6989(82)90007-4. [DOI] [PubMed] [Google Scholar]
  51. Orkand R. K., Nicholls J. G., Kuffler S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):788–806. doi: 10.1152/jn.1966.29.4.788. [DOI] [PubMed] [Google Scholar]
  52. Ostwald T. J., Steinberg R. H. Localization of frog retinal pigment epithelium Na+-K+ ATPase. Exp Eye Res. 1980 Sep;31(3):351–360. doi: 10.1016/s0014-4835(80)80043-1. [DOI] [PubMed] [Google Scholar]
  53. SKOU J. C. ENZYMATIC BASIS FOR ACTIVE TRANSPORT OF NA+ AND K+ ACROSS CELL MEMBRANE. Physiol Rev. 1965 Jul;45:596–617. doi: 10.1152/physrev.1965.45.3.596. [DOI] [PubMed] [Google Scholar]
  54. Saito Y., Wright E. M. Kinetics of the sodium pump in the frog choroid plexus. J Physiol. 1982 Jul;328:229–243. doi: 10.1113/jphysiol.1982.sp014261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. 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]
  56. Stirling C. E., Lee A. [3H]ouabain autoradiography of frog retina. J Cell Biol. 1980 May;85(2):313–324. doi: 10.1083/jcb.85.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. 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]
  58. Thomas R. C. Intracellular sodium activity and the sodium pump in snail neurones. J Physiol. 1972 Jan;220(1):55–71. doi: 10.1113/jphysiol.1972.sp009694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Tomita T. Electrophysiological studies of retinal cell function. Invest Ophthalmol. 1976 Mar;15(3):171–187. [PubMed] [Google Scholar]
  60. Torre V. The contribution of the electrogenic sodium-potassium pump to the electrical activity of toad rods. J Physiol. 1982 Dec;333:315–341. doi: 10.1113/jphysiol.1982.sp014456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Varon S. S., Somjen G. G. Neuron-glia interactions. Neurosci Res Program Bull. 1979 Feb;17(1):1–239. [PubMed] [Google Scholar]
  62. 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]
  63. Wise W. M., Kurey M. J., Baum G. Direct potentiometric measurement of potassium in blood serum with liquid ion-exchange electrode. Clin Chem. 1970 Feb;16(2):103–106. [PubMed] [Google Scholar]
  64. 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]
  65. Wuhrmann P., Ineichen H., Riesen-Willi U., Lezzi M. Change in nuclear potassium electrochemical activity and puffing of potassium-sensitive salivary chromosome regions during Chironomus development. Proc Natl Acad Sci U S A. 1979 Feb;76(2):806–808. doi: 10.1073/pnas.76.2.806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Zeuthen T., Wright E. M. Epithelial potassium transport: tracer and electrophysiological studies in choroid plexus. J Membr Biol. 1981;60(2):105–128. doi: 10.1007/BF01870414. [DOI] [PubMed] [Google Scholar]
  67. Zimmerman R. P., Corfman T. P. A comparison of the effects of isomers of alpha-aminoadipic acid and 2-amino-4-phosphonobutyric acid on the light response of the müller glial cell and the electroretinogram. Neuroscience. 1984 May;12(1):77–84. doi: 10.1016/0306-4522(84)90139-8. [DOI] [PubMed] [Google Scholar]

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