Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Mar;462:661–678. doi: 10.1113/jphysiol.1993.sp019575

Electrophysiological properties of axotomized facial motoneurones that are destined to die in neonatal rats.

M Umemiya 1, I Araki 1, M Kuno 1
PMCID: PMC1175321  PMID: 8392577

Abstract

1. Rat facial motoneurones axotomized on the day after birth were examined morphologically, and their electrical properties were characterized using the whole-cell recording technique in thin slices of the brainstem. 2. About 40% of facial motoneurones were lost within 4 days of axotomy, and only about 20% of the neurones survived 9 days after axotomy. 3. The surviving facial motoneurones examined 4 or 6 days after axotomy were reduced in size, and this was associated with a decrease in their input capacitance. 4. Both the resting potential and the amplitude of action potentials remained unchanged in axotomized facial motoneurones. 5. Facial motoneurones examined 4 or 6 days after axotomy showed an increase in the spike duration. When the preparation was superfused with a Ca(2+)-free solution, the spike duration of axotomized facial motoneurones was shortened, whereas the spike duration of control facial motoneurones was prolonged. 6. The voltage-gated transient K+ current (IA) density was significantly reduced in axotomized motoneurones, whereas the Ca(2+)-dependent transient K+ current (IK, Ca) density was not affected. 7. Voltage-gated Ca2+ currents in facial motoneurones showed inactivation, displaying an initial transient phase followed by a sustained phase. The rate of inactivation of Ca2+ currents was significantly faster in axotomized neurones than in control neurones. 8. A small subpopulation of facial motoneurones examined 4 or 6 days after axotomy had a disproportionately high input resistance and a significantly longer after-hyperpolarization. The probability of this occurring was correlated with the time course of cell death induced by axotomy. 9. It is concluded that facial motoneurones axotomized in neonatal rats comprise two subpopulations. The subpopulation characterized by a markedly high input resistance is suggested to represent the neurones which are at the 'prelethal' stage or in the process of cell death.

Full text

PDF
661

Images in this article

Selected References

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

  1. Adams P. R., Galvan M. Voltage-dependent currents of vertebrate neurons and their role in membrane excitability. Adv Neurol. 1986;44:137–170. [PubMed] [Google Scholar]
  2. Ashwell K. W., Watson C. R. The development of facial motoneurones in the mouse--neuronal death and the innervation of the facial muscles. J Embryol Exp Morphol. 1983 Oct;77:117–141. [PubMed] [Google Scholar]
  3. Berger A. J., Takahashi T. Serotonin enhances a low-voltage-activated calcium current in rat spinal motoneurons. J Neurosci. 1990 Jun;10(6):1922–1928. doi: 10.1523/JNEUROSCI.10-06-01922.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carlson J., Lais A. C., Dyck P. J. Axonal atrophy from permanent peripheral axotomy in adult cat. J Neuropathol Exp Neurol. 1979 Nov;38(6):579–585. doi: 10.1097/00005072-197911000-00002. [DOI] [PubMed] [Google Scholar]
  5. Choi D. W. Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1988 Oct;1(8):623–634. doi: 10.1016/0896-6273(88)90162-6. [DOI] [PubMed] [Google Scholar]
  6. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crews L. L., Wigston D. J. The dependence of motoneurons on their target muscle during postnatal development of the mouse. J Neurosci. 1990 May;10(5):1643–1653. doi: 10.1523/JNEUROSCI.10-05-01643.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Edwards F. A., Konnerth A., Sakmann B., Takahashi T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch. 1989 Sep;414(5):600–612. doi: 10.1007/BF00580998. [DOI] [PubMed] [Google Scholar]
  10. Foehring R. C., Sypert G. W., Munson J. B. Properties of self-reinnervated motor units of medial gastrocnemius of cat. II. Axotomized motoneurons and time course of recovery. J Neurophysiol. 1986 May;55(5):947–965. doi: 10.1152/jn.1986.55.5.947. [DOI] [PubMed] [Google Scholar]
  11. Kashihara Y., Kuno M., Miyata Y. Cell death of axotomized motoneurones in neonatal rats, and its prevention by peripheral reinnervation. J Physiol. 1987 May;386:135–148. doi: 10.1113/jphysiol.1987.sp016526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kuno M., Miyata Y., Muñoz-Martinez E. J. Properties of fast and slow alpha motoneurones following motor reinnervation. J Physiol. 1974 Oct;242(1):273–288. doi: 10.1113/jphysiol.1974.sp010706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kuno M. Target dependence of motoneuronal survival: the current status. Neurosci Res. 1990 Dec;9(3):155–172. doi: 10.1016/0168-0102(90)90001-u. [DOI] [PubMed] [Google Scholar]
  14. LAVELLE A., LAVELLE F. W. The nucleolar apparatus and neuronal reactivity to injury during development. J Exp Zool. 1958 Mar;137(2):285–315. doi: 10.1002/jez.1401370205. [DOI] [PubMed] [Google Scholar]
  15. Laiwand R., Werman R., Yarom Y. Electrophysiology of degenerating neurones in the vagal motor nucleus of the guinea-pig following axotomy. J Physiol. 1988 Oct;404:749–766. doi: 10.1113/jphysiol.1988.sp017317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Lowrie M. B., Krishnan S., Vrbová G. Permanent changes in muscle and motoneurones induced by nerve injury during a critical period of development of the rat. Brain Res. 1987 Jan;428(1):91–101. doi: 10.1016/0165-3806(87)90086-1. [DOI] [PubMed] [Google Scholar]
  20. Manabe T., Araki I., Takahashi T., Kuno M. Membrane currents recorded from sexually dimorphic motoneurones of the bulbocavernosus muscle in neonatal rats. J Physiol. 1991;440:419–435. doi: 10.1113/jphysiol.1991.sp018716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martin D. P., Schmidt R. E., DiStefano P. S., Lowry O. H., Carter J. G., Johnson E. M., Jr Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol. 1988 Mar;106(3):829–844. doi: 10.1083/jcb.106.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature. 1981 Jun 11;291(5815):497–500. doi: 10.1038/291497a0. [DOI] [PubMed] [Google Scholar]
  23. Oppenheim R. W., Prevette D., Tytell M., Homma S. Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: evidence for the role of cell death genes. Dev Biol. 1990 Mar;138(1):104–113. doi: 10.1016/0012-1606(90)90180-q. [DOI] [PubMed] [Google Scholar]
  24. Oppenheim R. W. The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. J Comp Neurol. 1986 Apr 8;246(2):281–286. doi: 10.1002/cne.902460211. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Romanes G. J. Motor localization and the effects of nerve injury on the ventral horn cells of the spinal cord. J Anat. 1946 Jul;80(Pt 3):117–131. [PMC free article] [PubMed] [Google Scholar]
  27. Sendtner M., Kreutzberg G. W., Thoenen H. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature. 1990 May 31;345(6274):440–441. doi: 10.1038/345440a0. [DOI] [PubMed] [Google Scholar]
  28. Siesjö B. K. Historical overview. Calcium, ischemia, and death of brain cells. Ann N Y Acad Sci. 1988;522:638–661. doi: 10.1111/j.1749-6632.1988.tb33410.x. [DOI] [PubMed] [Google Scholar]
  29. Snider W. D., Thanedar S. Target dependence of hypoglossal motor neurons during development in maturity. J Comp Neurol. 1989 Jan 15;279(3):489–498. doi: 10.1002/cne.902790312. [DOI] [PubMed] [Google Scholar]
  30. Søreide A. J. Variations in the axon reaction in animals of different ages. A light microscopic study on the facial nucleus of the rat. Acta Anat (Basel) 1981;110(1):40–47. [PubMed] [Google Scholar]
  31. Takahashi T. Membrane currents in visually identified motoneurones of neonatal rat spinal cord. J Physiol. 1990 Apr;423:27–46. doi: 10.1113/jphysiol.1990.sp018009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Titmus M. J., Faber D. S. Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog Neurobiol. 1990;35(1):1–51. doi: 10.1016/0301-0082(90)90039-j. [DOI] [PubMed] [Google Scholar]

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

RESOURCES