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. 1983 Aug 1;82(2):221–244. doi: 10.1085/jgp.82.2.221

The periaxonal space of crayfish giant axons

PMCID: PMC2228693  PMID: 6311939

Abstract

The influence of the glial cell layer on effective external ion concentrations has been studied in crayfish giant axons. Excess K ions accumulate in the periaxonal space during outward K+ current flow, but at a rate far below that expected from the total ionic flux and the measured thickness of the space. At the conclusion of outward current flow, the external K+ concentration returns to normal in an exponential fashion, with a time constant of approximately 2 ms. This process is about 25 times faster than is the case in squid axons. K+ repolarization (tail) currents are generally biphasic at potentials below about -40 mV and pass through a maximum before approaching a final asymptotic level. The initial rapid phase may in part reflect depletion of excess K+. After block of inactivation and reversal of the Na+ concentration gradient, we could demonstrate accumulation and washout of excess Na ions in the periaxonal space. Characteristics of these processes appeared similar to those of K+. Crayfish glial cell ultrastructure has been examined both in thin sections and after freeze fracture. Layers of connective tissue and extracellular fluid alternate with thin layers of glial cytoplasm. A membranous tubular lattice, spanning the innermost glial layers, may provide a pathway allowing rapid diffusion of excess ions from the axon surface.

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Selected References

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  1. ARMSTRONG C. M., BINSTOCK L. ANOMALOUS RECTIFICATION IN THE SQUID GIANT AXON INJECTED WITH TETRAETHYLAMMONIUM CHLORIDE. J Gen Physiol. 1965 May;48:859–872. doi: 10.1085/jgp.48.5.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adam G. The effect of potassium diffusion through the Schwann cell layer on potassium conductance of the squid axon. J Membr Biol. 1973 Nov 8;13(4):353–386. doi: 10.1007/BF01868236. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Armstrong C. M., Bezanilla F., Rojas E. Destruction of sodium conductance inactivation in squid axons perfused with pronase. J Gen Physiol. 1973 Oct;62(4):375–391. doi: 10.1085/jgp.62.4.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ballinger M. L., Bittner G. D. Ultrastructural studies of severed medial giant and other CNS axons in crayfish. Cell Tissue Res. 1980;208(1):123–133. doi: 10.1007/BF00234178. [DOI] [PubMed] [Google Scholar]
  6. Bezanilla F., Armstrong C. M. Inactivation of the sodium channel. I. Sodium current experiments. J Gen Physiol. 1977 Nov;70(5):549–566. doi: 10.1085/jgp.70.5.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Binstock L., Goldman L. Rectification in instantaneous potassium current-voltage relations in Myxicola giant axons. J Physiol. 1971 Sep;217(3):517–531. doi: 10.1113/jphysiol.1971.sp009583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dubois J. M., Bergman C. Potassium accumulation in the perinodal space of frog myelinated axons. Pflugers Arch. 1975 Jul 21;358(2):111–124. doi: 10.1007/BF00583922. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Dubois J. M. Simultaneous changes in the equilibrium potential and potassium conductance in voltage clamped Ranvier node in the frog. J Physiol. 1981 Sep;318:279–295. doi: 10.1113/jphysiol.1981.sp013864. [DOI] [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. Gardner-Medwin A. R. Possible roles of vertebrate neuroglia in potassium dynamics, spreading depression and migraine. J Exp Biol. 1981 Dec;95:111–127. doi: 10.1242/jeb.95.1.111. [DOI] [PubMed] [Google Scholar]
  13. Geren B. B., Schmitt F. O. THE STRUCTURE OF THE SCHWANN CELL AND ITS RELATION TO THE AXON IN CERTAIN INVERTEBRATE NERVE FIBERS. Proc Natl Acad Sci U S A. 1954 Sep;40(9):863–870. doi: 10.1073/pnas.40.9.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hille B. Potassium channels in myelinated nerve. Selective permeability to small cations. J Gen Physiol. 1973 Jun;61(6):669–686. doi: 10.1085/jgp.61.6.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Holtzman E., Freeman A. R., Kashner L. A. A cytochemical and electron microscope study of channels in the Schwann cells surrounding lobster giant axons. J Cell Biol. 1970 Feb;44(2):438–445. doi: 10.1083/jcb.44.2.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Keynes R. D., Bezanilla F., Taylor R. E., Rojas E. The rate of action of tetrodotoxin on sodium conductance in the squid giant axon. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):365–375. doi: 10.1098/rstb.1975.0016. [DOI] [PubMed] [Google Scholar]
  19. Krív N., Syková E., Vyklický L. Extracellular potassium changes in the spinal cord of the cat and their relation to slow potentials, active transport and impulse transmission. J Physiol. 1975 Jul;249(1):167–182. doi: 10.1113/jphysiol.1975.sp011009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lo M. V., Shrager P. Block and inactivation of sodium channels in nerve by amino acid derivatives. I. Dependence on voltage and sodium concentration. Biophys J. 1981 Jul;35(1):31–43. doi: 10.1016/S0006-3495(81)84772-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Meves H., Pichon Y. Proceedings: Effects of 4-aminopyridine on the potassium current in internally perfused giant axons of the squid. J Physiol. 1975 Sep;251(1):60P–62P. [PubMed] [Google Scholar]
  22. Moran N., Palti Y., Levitan E., Stämpfli R. Potassium ion accumulation at the external surface of the nodal membrane in frog myelinated fibers. Biophys J. 1980 Dec;32(3):939–954. doi: 10.1016/S0006-3495(80)85028-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nicholson C. Dynamics of the brain cell microenvironment. Neurosci Res Program Bull. 1980 Apr;18(2):175–322. [PubMed] [Google Scholar]
  24. Orkand R. K. Extracellular potassium accumulation in the nervous system. Fed Proc. 1980 Apr;39(5):1515–1518. [PubMed] [Google Scholar]
  25. 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]
  26. Peracchia C., Robertson J. D. Increase in osmiophilia of axonal membranes of crayfish as a result of electrical stimulation, asphyxia, or treatment with reducing agents. J Cell Biol. 1971 Oct;51(1):223–239. doi: 10.1083/jcb.51.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ritchie J. M., Rogart R. B. Density of sodium channels in mammalian myelinated nerve fibers and nature of the axonal membrane under the myelin sheath. Proc Natl Acad Sci U S A. 1977 Jan;74(1):211–215. doi: 10.1073/pnas.74.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schwarz J. R., Ulbricht W., Wagner H. H. The rate of action of tetrodotoxin on myelinated nerve fibres of Xenopus laevis and Rana esculenta. J Physiol. 1973 Aug;233(1):167–194. doi: 10.1113/jphysiol.1973.sp010304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shrager P. G., Macey R. I., Strickholm A. Internal perfusion of crayfish, giant axons: action of tannic acid, DDT, and TEA. J Cell Physiol. 1969 Aug;74(1):77–90. doi: 10.1002/jcp.1040740111. [DOI] [PubMed] [Google Scholar]
  30. Shrager P. Ionic conductance changes in voltage clamped crayfish axons at low pH. J Gen Physiol. 1974 Dec;64(6):666–690. doi: 10.1085/jgp.64.6.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shrager P., Lo M. V. Influence of ionic current on Na+ channel gating in crayfish giant axon. Nature. 1982 Apr 1;296(5856):450–452. doi: 10.1038/296450a0. [DOI] [PubMed] [Google Scholar]
  32. Shrager P. Specific chemical groups involved in the control of ionic conductance in nerve. Ann N Y Acad Sci. 1975 Dec 30;264:293–303. doi: 10.1111/j.1749-6632.1975.tb31490.x. [DOI] [PubMed] [Google Scholar]
  33. Starkus J. G., Shrager P. Modification of slow sodium inactivation in nerve after internal perfusion with trypsin. Am J Physiol. 1978 Nov;235(5):C238–C244. doi: 10.1152/ajpcell.1978.235.5.C238. [DOI] [PubMed] [Google Scholar]
  34. Tang C. M., Strichartz G. R., Orkand R. K. Sodium channels in axons and glial cells of the optic nerve of Necturus maculosa. J Gen Physiol. 1979 Nov;74(5):629–642. doi: 10.1085/jgp.74.5.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Taylor R. E., Bezanilla F., Rojas E. Diffusion models for the squid axon Schwann cell layer. Biophys J. 1980 Jan;29(1):95–117. doi: 10.1016/S0006-3495(80)85120-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. VILLEGAS R., VILLEGAS G. M. Characterization of the membranes in the giant nerve fiber of the squid. J Gen Physiol. 1960 May;43:73–103. doi: 10.1085/jgp.43.5.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Varon S. S., Somjen G. G. Neuron-glia interactions. Neurosci Res Program Bull. 1979 Feb;17(1):1–239. [PubMed] [Google Scholar]
  38. Villegas G. M. Electron microscopic study of the giant nerve fiber of the giant squid Dosidicus gigas. J Ultrastruct Res. 1969 Mar;26(5):501–504. doi: 10.1016/s0022-5320(69)90054-9. [DOI] [PubMed] [Google Scholar]
  39. Wallin G. Simultaneous determination of membrane potential and intracellular ion concentrations in single nerve axons. Nature. 1966 Oct 29;212(5061):521–522. doi: 10.1038/212521a0. [DOI] [PubMed] [Google Scholar]
  40. Yeh J. Z., Oxford G. S., Wu C. H., Narahashi T. Interactions of aminopyridines with potassium channels of squid axon membranes. Biophys J. 1976 Jan;16(1):77–81. doi: 10.1016/S0006-3495(76)85663-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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