Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1983 Jan;334:225–244. doi: 10.1113/jphysiol.1983.sp014491

Effects of extracellular potassium concentration on the excitability of the parallel fibres of the rat cerebellum.

J D Kocsis, R C Malenka, S G Waxman
PMCID: PMC1197311  PMID: 6864558

Abstract

1. Field potentials and extracellular potassium concentration, [K+]o, were recorded from the rat cerebellar cortex using ion-selective micro-electrodes, following micro-stimulation of the cerebellar surface. The compound action potential of the parallel fibres (p.f.s) showed changes indicative of a supernormal period (s.n.p) when conditioned by a previous p.f. volley, and was studied in relation to [K+]o. 2. Repetitive stimulation of the p.f.s (greater than 10 Hz) elicited an alternation in p.f. excitability from supernormality to subnormality simultaneous to a steady increase in [K+]o. 3. Superfusion with various levels of K+ led to changes in the p.f. conduction properties. Small increases in [K+]o above the resting 3.0 mM level led to an increase in p.f. conduction velocity while greater increases led to conduction slowing and eventually block. 4. Repetitive activation of a row of p.f.s elicited increases in [K+]o in the vicinity of neighbouring non-activated fibres. These fibres displayed an increase in excitability that was quantitatively related to [K+]o. 5. After introduction of 4-aminopyridine (4-AP; 100 microM) into the superfusate, a single stimulus would elicit relatively large (up to 15 mM) increases in [K+]o around neighbouring non-activated p.f.s. The excitability of the adjacent non-activated fibres was either increased or decreased, and was quantitatively related to [K+]o. 6. Strophanthidin application (15 microM) led to a slow and continuous increase in [K+]o. The excitability of the p.f.s initially increased as [K+]o increased, but subsequently decreased, eventually resulting in conduction block. 7. These experiments are consistent with the hypothesis that small increases in [K+]o may elicit an increase in p.f. excitability while greater increases lead to a decrease in p.f. excitability.

Full text

PDF
225

Selected References

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

  1. Adelman W. J., Jr, Palti Y., Senft J. P. Potassium ion accumulation in a periaxonal space and its effect on the measurement of membrane potassium ion conductance. J Membr Biol. 1973 Nov 8;13(4):387–410. doi: 10.1007/BF01868237. [DOI] [PubMed] [Google Scholar]
  2. Baldissera F., Gustafsson B. Firing behaviour of a neurone model based on the afterhyperpolarization conductance time course. First interval firing. Acta Physiol Scand. 1974 Aug;91(4):528–544. doi: 10.1111/j.1748-1716.1974.tb05708.x. [DOI] [PubMed] [Google Scholar]
  3. Baylor D. A., Nicholls J. G. Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech. J Physiol. 1969 Aug;203(3):555–569. doi: 10.1113/jphysiol.1969.sp008879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bliss T. V., Rosenberg M. E. Activity-dependent changes in conduction velocity in the olfactory nerve of the tortoise. Pflugers Arch. 1979 Sep;381(3):209–216. doi: 10.1007/BF00583251. [DOI] [PubMed] [Google Scholar]
  5. Brismar T. Potential clamp analysis of membrane currents in rat myelinated nerve fibres. J Physiol. 1980 Jan;298:171–184. doi: 10.1113/jphysiol.1980.sp013074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chiu S. Y., Ritchie J. M., Rogart R. B., Stagg D. A quantitative description of membrane currents in rabbit myelinated nerve. J Physiol. 1979 Jul;292:149–166. doi: 10.1113/jphysiol.1979.sp012843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cordingley G. E., Somjen G. G. The clearing of excess potassium from extracellular space in spinal cord and cerebral cortex. Brain Res. 1978 Aug 4;151(2):291–306. doi: 10.1016/0006-8993(78)90886-7. [DOI] [PubMed] [Google Scholar]
  8. Cummins K. L., Perkel D. H., Dorfman L. J. Nerve fiber conduction-velocity distributions. I. Estimation based on the single-fiber and compound action potentials. Electroencephalogr Clin Neurophysiol. 1979 Jun;46(6):634–646. doi: 10.1016/0013-4694(79)90101-9. [DOI] [PubMed] [Google Scholar]
  9. Eccles J. C., Llinás R., Sasaki K. Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp Brain Res. 1966;1(1):17–39. doi: 10.1007/BF00235207. [DOI] [PubMed] [Google Scholar]
  10. FOX C. A., BARNARD J. W. A quantitative study of the Purkinje cell dendritic branchlets and their relationship to afferent fibres. J Anat. 1957 Jul;91(3):299–313. [PMC free article] [PubMed] [Google Scholar]
  11. FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Gardner-Medwin A. R. An extreme supernormal period in cerebellar parallel fibres. J Physiol. 1972 Apr;222(2):357–371. doi: 10.1113/jphysiol.1972.sp009802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gillespie J. I., Meves H. The effect of external potassium on the removal of sodium inactivation in squid giant axons. J Physiol. 1981 Jun;315:493–514. doi: 10.1113/jphysiol.1981.sp013760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grossman Y., Parnas I., Spira M. E. Mechanisms involved in differential conduction of potentials at high frequency in a branching axon. J Physiol. 1979 Oct;295:307–322. doi: 10.1113/jphysiol.1979.sp012970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kocsis J. D., Cummins K. L., Waxman S. G., Malenka R. C. Impulse entrainment: computer simulations and studies on the parallel fibers of the cerebellum. Exp Neurol. 1981 Jun;72(3):628–637. doi: 10.1016/0014-4886(81)90011-x. [DOI] [PubMed] [Google Scholar]
  17. Kocsis J. D., Malenka R. C., Waxman S. G. Enhanced parallel fiber frequency-following after reduction of postsynaptic activity. Brain Res. 1981 Mar 2;207(2):321–331. doi: 10.1016/0006-8993(81)90367-x. [DOI] [PubMed] [Google Scholar]
  18. Kocsis J. D., Waxman S. G. Absence of potassium conductance in central myelinated axons. Nature. 1980 Sep 25;287(5780):348–349. doi: 10.1038/287348a0. [DOI] [PubMed] [Google Scholar]
  19. Krnjević K., Morris M. E. Factors determining the decay of K+ potentials and focal potentials in the central nervous system. Can J Physiol Pharmacol. 1975 Oct;53(5):923–934. doi: 10.1139/y75-126. [DOI] [PubMed] [Google Scholar]
  20. Kríz N., Syková E., Ujec E., Vyklický L. Changes of extracellular potassium concentration induced by neuronal activity in the sinal cord of the cat. J Physiol. 1974 Apr;238(1):1–15. doi: 10.1113/jphysiol.1974.sp010507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol. 1980 Aug;305:197–213. doi: 10.1113/jphysiol.1980.sp013358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol. 1980 Aug;305:171–195. doi: 10.1113/jphysiol.1980.sp013357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lothman E. W., Somjen G. G. Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord. J Physiol. 1975 Oct;252(1):115–136. doi: 10.1113/jphysiol.1975.sp011137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lux H. D., Neher E. The equilibration time course of (K + ) 0 in cat cortex. Exp Brain Res. 1973 Apr 30;17(2):190–205. doi: 10.1007/BF00235028. [DOI] [PubMed] [Google Scholar]
  25. Malenka R. C., Kocsis J. D., Ransom B. R., Waxman S. G. Modulation of parallel fiber excitability by postsynaptically mediated changes in extracellular potassium. Science. 1981 Oct 16;214(4518):339–341. doi: 10.1126/science.7280695. [DOI] [PubMed] [Google Scholar]
  26. Merrill E. G., Wall P. D., Yaksh T. L. Properties of two unmyelinated fibre tracts of the central nervous system: lateral Lissauer tract, and parallel fibres of the cerebellum. J Physiol. 1978 Nov;284:127–145. doi: 10.1113/jphysiol.1978.sp012531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nicholson C., Bruggencate G. T., Senekowitsch R. Large potassium signals and slow potentials evoked during aminopyridine or barium superfusion in cat cerebellum. Brain Res. 1976 Sep 3;113(3):606–610. doi: 10.1016/0006-8993(76)90063-9. [DOI] [PubMed] [Google Scholar]
  28. Nicholson C., Kraig R. P. Chloride and potassium changes measured during spreading depression in catfish cerebellum. Brain Res. 1975 Oct 17;96(2):384–389. doi: 10.1016/0006-8993(75)90752-0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Nicoll R. A. Dorsal root potentials and changes in extracellular potassium in the spinal cord of the frog. J Physiol. 1979 May;290(2):113–127. doi: 10.1113/jphysiol.1979.sp012763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Orkand R. K. Extracellular potassium accumulation in the nervous system. Fed Proc. 1980 Apr;39(5):1515–1518. [PubMed] [Google Scholar]
  32. Raymond S. A. Effects of nerve impulses on threshold of frog sciatic nerve fibres. J Physiol. 1979 May;290(2):273–303. doi: 10.1113/jphysiol.1979.sp012771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Smith D. O. Mechanisms of action potential propagation failure at sites of axon branching in the crayfish. J Physiol. 1980 Apr;301:243–259. doi: 10.1113/jphysiol.1980.sp013202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Spear J. F., Moore E. N. Supernormal excitability and conduction in the His-Purkinje system of the dog. Circ Res. 1974 Nov;35(5):782–792. doi: 10.1161/01.res.35.5.782. [DOI] [PubMed] [Google Scholar]
  36. Syková E., Orkand R. K. Extracellular potassium accumulation and transmission in frog spinal cord. Neuroscience. 1980;5(8):1421–1428. doi: 10.1016/0306-4522(80)90003-2. [DOI] [PubMed] [Google Scholar]
  37. Thomas R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol Rev. 1972 Jul;52(3):563–594. doi: 10.1152/physrev.1972.52.3.563. [DOI] [PubMed] [Google Scholar]
  38. Weight F. F., Erulkar S. D. Modulation of synaptic transmitter release by repetitive postsynaptic action potentials. Science. 1976 Sep 10;193(4257):1023–1025. doi: 10.1126/science.7839. [DOI] [PubMed] [Google Scholar]
  39. Zucker R. S. Excitability changes in crayfish motor neurone terminals. J Physiol. 1974 Aug;241(1):111–126. doi: 10.1113/jphysiol.1974.sp010643. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES