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. 1989 Sep;416:93–110. doi: 10.1113/jphysiol.1989.sp017751

Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres.

J Röper 1, J R Schwarz 1
PMCID: PMC1189205  PMID: 2558178

Abstract

1. Potassium currents were measured in voltage-clamped single myelinated rat nerve fibres before and after paranodal demyelination with 0.2% pronase or 0.2% lysolecithin added to the external solution. Sodium currents were blocked by 300 nM-tetrodotoxin. For the purpose of comparison, intact frog nerve fibres were also investigated. 2. Our results suggest the existence of at least two distinct types of K+ channels in the intact node of Ranvier, one with slow and another with fast gating kinetics, in the ratio 4:1. 3. In the rat nodal membrane, slow K+ channels have voltage-dependent time constants of K+ deactivation with tau n = 68 ms at E = -105 mV and tau n = 26 ms at E = -150 mV at 20 degrees C. The activation curve of the slow K+ conductance is sigmoid with an inflexion point at -60 mV. This means that about 35% of the slow K+ channels are in the open state at the resting potential of -77 mV. Slow K+ channels could be blocked by 10 mM-tetraethylammonium chloride, but were insensitive to 4-aminopyridine. 4. After paranodal demyelination the ratio of fast to slow K+ channels increased from 17 to 83%. As in the frog (Dubois, 1981 alpha), the population of fast K+ channels in the rat may consist of two different subgroups, both of which can be blocked by 4-aminopyridine. 5. Demyelination was accompanied by an increase in the capacity current which was used to estimate the exposed membrane area. The density of slow and fast K+ channels was calculated from the quotient of the steady-state K+ conductance to membrane area. The density of the slow K+ channels is maximal in the nodal membrane and decreases to 1/31 in the internode. By contrast, the distribution of the fast K+ channels differs, their density being maximal in the paranode and decreasing to one-sixth in the node and internode.

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Selected References

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  1. Baker M., Bostock H., Grafe P., Martius P. Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J Physiol. 1987 Feb;383:45–67. doi: 10.1113/jphysiol.1987.sp016395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berthold C. H., Rydmark M. Electrophysiology and morphology of myelinated nerve fibers. VI. Anatomy of the paranode-node-paranode region in the cat. Experientia. 1983 Sep 15;39(9):964–976. doi: 10.1007/BF01989761. [DOI] [PubMed] [Google Scholar]
  3. Binah O., Palti Y. Potassium channels in the nodal membrane of rat myelinated fibres. Nature. 1981 Apr 16;290(5807):598–600. doi: 10.1038/290598a0. [DOI] [PubMed] [Google Scholar]
  4. Brismar T. Electrical properties of isolated demyelinated rat nerve fibres. Acta Physiol Scand. 1981 Oct;113(2):161–166. doi: 10.1111/j.1748-1716.1981.tb06877.x. [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. Brismar T. Potential clamp experiments on myelinated nerve fibres from alloxan diabetic rats. Acta Physiol Scand. 1979 Mar;105(3):384–386. doi: 10.1111/j.1748-1716.1979.tb06356.x. [DOI] [PubMed] [Google Scholar]
  7. Brismar T., Schwarz J. R. Potassium permeability in rat myelinated nerve fibres. Acta Physiol Scand. 1985 Jun;124(2):141–148. doi: 10.1111/j.1748-1716.1985.tb07645.x. [DOI] [PubMed] [Google Scholar]
  8. Chiu S. Y., Ritchie J. M. Evidence for the presence of potassium channels in the internode of frog myelinated nerve fibres. J Physiol. 1982 Jan;322:485–501. doi: 10.1113/jphysiol.1982.sp014051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chiu S. Y., Ritchie J. M. Evidence for the presence of potassium channels in the paranodal region of acutely demyelinated mammalian single nerve fibres. J Physiol. 1981;313:415–437. doi: 10.1113/jphysiol.1981.sp013674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chiu S. Y., Ritchie J. M. On the physiological role of internodal potassium channels and the security of conduction in myelinated nerve fibres. Proc R Soc Lond B Biol Sci. 1984 Feb 22;220(1221):415–422. doi: 10.1098/rspb.1984.0010. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Chiu S. Y., Schwarz W. Sodium and potassium currents in acutely demyelinated internodes of rabbit sciatic nerves. J Physiol. 1987 Oct;391:631–649. doi: 10.1113/jphysiol.1987.sp016760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dubois J. M. Capsaicin blocks one class of K+ channels in the frog node of Ranvier. Brain Res. 1982 Aug 12;245(2):372–375. doi: 10.1016/0006-8993(82)90820-4. [DOI] [PubMed] [Google Scholar]
  14. Dubois J. M. Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane. J Physiol. 1981 Sep;318:297–316. doi: 10.1113/jphysiol.1981.sp013865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dubois J. M. Properties of the slow K+ current of the nodal membrane. J Physiol (Paris) 1981 May;77(9):1129–1134. [PubMed] [Google Scholar]
  16. Grissmer S. Properties of potassium and sodium channels in frog internode. J Physiol. 1986 Dec;381:119–134. doi: 10.1113/jphysiol.1986.sp016317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Howe J. R., Ritchie J. M. Two types of potassium current in rabbit cultured Schwann cells. Proc R Soc Lond B Biol Sci. 1988 Oct 22;235(1278):19–27. doi: 10.1098/rspb.1988.0061. [DOI] [PubMed] [Google Scholar]
  18. Kocsis J. D., Waxman S. G., Hildebrand C., Ruiz J. A. Regenerating mammalian nerve fibres: changes in action potential waveform and firing characteristics following blockage of potassium conductance. Proc R Soc Lond B Biol Sci. 1982 Dec 22;217(1206):77–87. doi: 10.1098/rspb.1982.0095. [DOI] [PubMed] [Google Scholar]
  19. Kocsis J. D., Waxman S. G. Ionic channel organization of normal and regenerating mammalian axons. Prog Brain Res. 1987;71:89–101. doi: 10.1016/s0079-6123(08)61816-6. [DOI] [PubMed] [Google Scholar]
  20. Krylov B. V., Makovsky V. S. Spike frequency adaptation in amphibian sensory fibres is probably due to slow K channels. Nature. 1978 Oct 12;275(5680):549–551. doi: 10.1038/275549a0. [DOI] [PubMed] [Google Scholar]
  21. Lasek R. J., Tytell M. A. Macromolecular transfer from glia to the axon. J Exp Biol. 1981 Dec;95:153–165. doi: 10.1242/jeb.95.1.153. [DOI] [PubMed] [Google Scholar]
  22. Neumcke B., Schwarz J. R., Stämpfli R. A comparison of sodium currents in rat and frog myelinated nerve: normal and modified sodium inactivation. J Physiol. 1987 Jan;382:175–191. doi: 10.1113/jphysiol.1987.sp016362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Neumcke B., Stämpfli R. Sodium currents and sodium-current fluctuations in rat myelinated nerve fibres. J Physiol. 1982 Aug;329:163–184. doi: 10.1113/jphysiol.1982.sp014296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nonner W. A new voltage clamp method for Ranvier nodes. Pflugers Arch. 1969;309(2):176–192. doi: 10.1007/BF00586967. [DOI] [PubMed] [Google Scholar]
  25. Schwarz J. R., Eikhof G. Na currents and action potentials in rat myelinated nerve fibres at 20 and 37 degrees C. Pflugers Arch. 1987 Aug;409(6):569–577. doi: 10.1007/BF00584655. [DOI] [PubMed] [Google Scholar]
  26. Schwarz J. R., Vogel W. Potassium inactivation in single myelinated nerve fibres of Xenopus laevis. Pflugers Arch. 1971;330(1):61–73. doi: 10.1007/BF00588735. [DOI] [PubMed] [Google Scholar]
  27. Sherratt R. M., Bostock H., Sears T. A. Effects of 4-aminopyridine on normal and demyelinated mammalian nerve fibres. Nature. 1980 Feb 7;283(5747):570–572. doi: 10.1038/283570a0. [DOI] [PubMed] [Google Scholar]
  28. Shrager P., Chiu S. Y., Ritchie J. M. Voltage-dependent sodium and potassium channels in mammalian cultured Schwann cells. Proc Natl Acad Sci U S A. 1985 Feb;82(3):948–952. doi: 10.1073/pnas.82.3.948. [DOI] [PMC free article] [PubMed] [Google Scholar]

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