Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1972 Sep;225(2):275–296. doi: 10.1113/jphysiol.1972.sp009940

Axon-schwann cell interaction in the squid nerve fibre

Jorge Villegas
PMCID: PMC1331106  PMID: 5074387

Abstract

The electrical properties of Schwann cells and the effects of neuronal impulses on their membrane potential have been studied in the giant nerve fibre of the squid.

1. The behaviour of the Schwann cell membrane to current injection into the cell was ohmic. No impulse-like responses were observed with displacements of 35 mV in the membrane potential. The resistance of the Schwann cell membrane was found to be approximately 103 Ω cm2.

2. A long-lasting hyperpolarization is observed in the Schwann cells following the conduction of impulse trains by the axon. Whereas the propagation of a single impulse had little effect, prolonged stimulation of the fibre at 250 impulses/sec was followed by a hyperpolarization of the Schwann cell that gradually declined over a period of several minutes.

3. The prolonged effects of nerve impulse trains on the Schwann cell were similar to those produced by depolarizing current pulses applied to the axon by the voltage-clamp technique. Thus, a series of depolarizing pulses in the axon was followed by a long-lasting hyperpolarization of the Schwann cells. In contrast, the application of a series of hyperpolarizing 100 mV pulses at a frequency of 1/sec had no apparent effects.

4. Changes in the external potassium concentration did not reproduce the long-lasting effects of nerve excitation.

5. The hyperpolarizing effects of impulse trains were abolished by the incubation of the nerve fibre in a sea-water solution containing trypsin.

6. These findings are discussed in relation to the possible mechanisms that might be responsible for the long-lasting hyperpolarizations of the Schwann cells.

Full text

PDF
275

Selected References

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

  1. ARAKI T., OTANI T. Response of single motoneurons to direct stimulation in toad's spinal cord. J Neurophysiol. 1955 Sep;18(5):472–485. doi: 10.1152/jn.1955.18.5.472. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Ehrenstein G., Gilbert D. L. Slow changes of potassium permeability in the squid giant axon. Biophys J. 1966 Sep;6(5):553–566. doi: 10.1016/S0006-3495(66)86677-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. KUFFLER S. W., POTTER D. D. GLIA IN THE LEECH CENTRAL NERVOUS SYSTEM: PHYSIOLOGICAL PROPERTIES AND NEURON-GLIA RELATIONSHIP. J Neurophysiol. 1964 Mar;27:290–320. doi: 10.1152/jn.1964.27.2.290. [DOI] [PubMed] [Google Scholar]
  7. Kuffler S. W., Nicholls J. G., Orkand R. K. Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):768–787. doi: 10.1152/jn.1966.29.4.768. [DOI] [PubMed] [Google Scholar]
  8. Loewenstein W. R., Nakas M., Socolar S. J. Junctional membrane uncoupling. Permeability transformations at a cell membrane junction. J Gen Physiol. 1967 Aug;50(7):1865–1891. doi: 10.1085/jgp.50.7.1865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. NICHOLLS J. G., KUFFLER S. W. EXTRACELLULAR SPACE AS A PATHWAY FOR EXCHANGE BETWEEN BLOOD AND NEURONS IN THE CENTRAL NERVOUS SYSTEM OF THE LEECH: IONIC COMPOSITION OF GLIAL CELLS AND NEURONS. J Neurophysiol. 1964 Jul;27:645–671. doi: 10.1152/jn.1964.27.4.645. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. TOBIAS J. M. Further studies on the nature of the excitable system in nerve. I. Voltage-induced axoplasm movement in squid axons. II. Penetration of surviving, excitable axons by proteases. III. Effects of proteases and of phospholipases on lobster giant axon resistance and capacity. J Gen Physiol. 1960 May;43:57–71. doi: 10.1085/jgp.43.5.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Takenaka T., Yamagishi S. Morphology and electrophysiological properties of squid giant axons perfused intracellularly with protease solution. J Gen Physiol. 1969 Jan;53(1):81–96. doi: 10.1085/jgp.53.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. VILLEGAS G. M., VILLEGAS R. The ultrastructure of the giant nerve fibre of the squid: axon-Schwann cell relationship. J Ultrastruct Res. 1960 Jun;3:362–373. doi: 10.1016/s0022-5320(60)90015-0. [DOI] [PubMed] [Google Scholar]
  14. VILLEGAS R., BARNOLA F. V. Characterization of the resting axolemma in the giant axon of the squid. J Gen Physiol. 1961 May;44:963–977. doi: 10.1085/jgp.44.5.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. VILLEGAS R., CAPUTO C., VILLEGAS L. Diffusion barrieres in the squid nerve fiber. The axolemma and the Schwann layer. J Gen Physiol. 1962 Nov;46:245–255. doi: 10.1085/jgp.46.2.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. VILLEGAS R., VILLEGAS L., GIMENEZ M., VILLEGAS G. M. Schwann cell and axon electrical potential differences. Squid nerve structure and excitable membrane location. J Gen Physiol. 1963 May;46:1047–1064. doi: 10.1085/jgp.46.5.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Villegas G. M., Villegas R. Ultrastructural studies of the squid nerve fibers. J Gen Physiol. 1968 May 1;51(5):44–60. [PMC free article] [PubMed] [Google Scholar]
  19. Villegas J. Transport of electrolytes in the schwann cell and location of sodium by electron microscopy. J Gen Physiol. 1968 May 1;51(5):61–71. [PMC free article] [PubMed] [Google Scholar]
  20. Villegas J., Villegas L., Villegas R. Sodium, potassium, and chloride concentrations in the Schwann cell and axon of the squid nerve fiber. J Gen Physiol. 1965 Sep;49(1):1–7. doi: 10.1085/jgp.49.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Villegas J., Villegas R., Giménez M. Nature of the Schwann cell electrical potential. Effects of the external ionic concentrations and a cardiac glycoside. J Gen Physiol. 1968 Jan;51(1):47–64. doi: 10.1085/jgp.51.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES