Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Oct;404:749–766. doi: 10.1113/jphysiol.1988.sp017317

Electrophysiology of degenerating neurones in the vagal motor nucleus of the guinea-pig following axotomy.

R Laiwand 1, R Werman 1, Y Yarom 1
PMCID: PMC1190853  PMID: 2855353

Abstract

1. The electrophysiological properties of motoneurones in the dorsal motor nucleus of the vagus in the guinea-pig were studied at different times following cervical vagotomy. The results were compared both to normal neurones and to results obtained at the same time from intact neurones located in the contralateral nucleus. 2. The input resistances of axotomized neurones are significantly higher than those of normal neurones (66 +/- 29 compared to 45 +/- 17 M omega). This difference was seen during the first month following axotomy without any sign of a time-dependent process. On the other hand, no change in resting potential was observed. 3. Significant reduction in action potential amplitude was observed 1 month after axotomy (from 97.8 +/- 8 to 87 +/- 7 mV) and was followed by slow recovery lasting more than 1 year. Neither the Na+ conductance nor the voltage-dependent K+ conductance responsible for the fast rise and fall of the action potential, respectively, were affected by axotomy. 4. One month after axotomy the action potential duration in axotomized neurones was found to be shorter than that of normal neurones (0.9 +/- 0.1 ms compared to 1.1 +/- 0.04 ms). We show that this decrease in duration reflects a reduction in the depolarizing hump on the falling phase of the action potential, which is known to express the Ca2+ conductance activated during the action potential. A slow recovery of the spike duration was observed, although an age-dependent reduction in duration was also observed in neurones in the contralateral nucleus. 5. Two K+ conductances, the Ca2+-dependent and the A type, decrease 1 month after axotomy and follow a similar time course of recovery to that of the reduction in action potential duration and amplitude. 6. The firing pattern of axotomized neurones undergoes profound alteration, manifested as an increase in firing duration as a response to a rectangular current pulse. Examination of these alterations reveals that the reduction in both K+ conductances is responsible for the observed changes. 7. The results are discussed within the framework of the degenerative response known to take place in the nucleus following axotomy. We hypothesize that the observed phenomena reflect an increase in intracellular Ca2+ concentration which, in turn, inactivates the Ca2+ and K+ conductances. Furthermore this rise in intracellular Ca2+ may eventually be responsible for cell death.

Full text

PDF
749

Selected References

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

  1. Alkon D. L., Shoukimas J. J., Heldman E. Calcium-mediated decrease of a voltage-dependent potassium current. Biophys J. 1982 Dec;40(3):245–250. doi: 10.1016/S0006-3495(82)84479-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Choi D. W. Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci Lett. 1985 Aug 5;58(3):293–297. doi: 10.1016/0304-3940(85)90069-2. [DOI] [PubMed] [Google Scholar]
  3. ECCLES J. C., LIBET B., YOUNG R. R. The behaviour of chromatolysed motoneurones studied by intracellular recording. J Physiol. 1958 Aug 29;143(1):11–40. doi: 10.1113/jphysiol.1958.sp006041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eckert R., Ewald D. Residual calcium ions depress activation of calcium-dependent current. Science. 1982 May 14;216(4547):730–733. doi: 10.1126/science.6281880. [DOI] [PubMed] [Google Scholar]
  5. Eckert R., Tillotson D. L., Brehm P. Calcium-mediated control of Ca and K currents. Fed Proc. 1981 Jun;40(8):2226–2232. [PubMed] [Google Scholar]
  6. Farber J. L. The role of calcium in cell death. Life Sci. 1981 Sep 28;29(13):1289–1295. doi: 10.1016/0024-3205(81)90670-6. [DOI] [PubMed] [Google Scholar]
  7. Garthwaite G., Garthwaite J. Amino acid neurotoxicity: intracellular sites of calcium accumulation associated with the onset of irreversible damage to rat cerebellar neurones in vitro. Neurosci Lett. 1986 Oct 30;71(1):53–58. doi: 10.1016/0304-3940(86)90256-9. [DOI] [PubMed] [Google Scholar]
  8. Hermann A., Hartung K. Properties of a Ca2+ activated K+ conductance in Helix neurones investigated by intracellular Ca2+ ionophoresis. Pflugers Arch. 1982 May;393(3):248–253. doi: 10.1007/BF00584078. [DOI] [PubMed] [Google Scholar]
  9. Heyer C. B., Llinás R. Control of rhythmic firing in normal and axotomized cat spinal motoneurons. J Neurophysiol. 1977 May;40(3):480–488. doi: 10.1152/jn.1977.40.3.480. [DOI] [PubMed] [Google Scholar]
  10. Kuno M., Llinás R. Alterations of synaptic action in chromatolysed motoneurones of the cat. J Physiol. 1970 Nov;210(4):823–838. doi: 10.1113/jphysiol.1970.sp009244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kuno M., Llinás R. Enhancement of synaptic transmission by dendritic potentials in chromatolysed motoneurones of the cat. J Physiol. 1970 Nov;210(4):807–821. doi: 10.1113/jphysiol.1970.sp009243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Laiwand R., Werman R., Yarom Y. Time course and distribution of motoneuronal loss in the dorsal motor vagal nucleus of guinea pig after cervical vagotomy. J Comp Neurol. 1987 Feb 22;256(4):527–537. doi: 10.1002/cne.902560405. [DOI] [PubMed] [Google Scholar]
  13. Lee K. S., Marban E., Tsien R. W. Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium. J Physiol. 1985 Jul;364:395–411. doi: 10.1113/jphysiol.1985.sp015752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Levitan E. S., Levitan I. B. Apparent loss of calcium-activated potassium current in internally perfused snail neurons is due to accumulation of free intracellular calcium. J Membr Biol. 1986;90(1):59–65. doi: 10.1007/BF01869686. [DOI] [PubMed] [Google Scholar]
  15. Lieberman A. R. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol. 1971;14:49–124. doi: 10.1016/s0074-7742(08)60183-x. [DOI] [PubMed] [Google Scholar]
  16. Llinás R., Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol. 1981 Jun;315:549–567. doi: 10.1113/jphysiol.1981.sp013763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Plant T. D., Standen N. B. Calcium current inactivation in identified neurones of Helix aspersa. J Physiol. 1981 Dec;321:273–285. doi: 10.1113/jphysiol.1981.sp013983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Siesjö B. K. Cell damage in the brain: a speculative synthesis. J Cereb Blood Flow Metab. 1981;1(2):155–185. doi: 10.1038/jcbfm.1981.18. [DOI] [PubMed] [Google Scholar]
  19. Stein R. B. The frequency of nerve action potentials generated by applied currents. Proc R Soc Lond B Biol Sci. 1967 Jan 31;167(1006):64–86. doi: 10.1098/rspb.1967.0013. [DOI] [PubMed] [Google Scholar]
  20. Tokimasa T. Intracellular Ca2+-ions inactivate K+-current in bullfrog sympathetic neurons. Brain Res. 1985 Jul 1;337(2):386–391. doi: 10.1016/0006-8993(85)90081-2. [DOI] [PubMed] [Google Scholar]
  21. Yarom Y., Sugimori M., Llinás R. Ionic currents and firing patterns of mammalian vagal motoneurons in vitro. Neuroscience. 1985 Dec;16(4):719–737. doi: 10.1016/0306-4522(85)90090-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES