Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1991 Sep;441:405–421. doi: 10.1113/jphysiol.1991.sp018758

Neuromuscular transmission at newly formed neuromuscular junctions in the regenerating soleus muscle of the rat.

B D Grubb 1, J B Harris 1, I S Schofield 1
PMCID: PMC1180205  PMID: 1667798

Abstract

1. A study of neuromuscular function in regenerating skeletal muscle fibres in the rat soleus muscle has been made. The muscle fibres were damaged in vivo by the injection of the myotoxic venom component notexin, and then allowed to regenerate spontaneously. 2. Regenerating muscle fibres generated action potentials and contracted following direct intracellular stimulation as early as 4 days after the injection of notexin. 3. Miniature endplate potentials (MEPPs) were recorded at a minority of synapses at 3 days, and from all synapses by 5 days. The mean amplitude of MEPPs in a given fibre was directly proportional to muscle fibre input resistance. 4. Spontaneous transmitter release in the regenerating fibres was relatively insensitive to changes in [K+]0 but the effect of Ruthenium Red on spontaneous release was similar in the regenerating and control muscle fibres. 5. Functional innervation, defined as the ability to generate an indirect action potential, was restored in 97% of fibres by 10 days. The generation of an action potential was always associated with a twitch of the muscle fibre. Those fibres that were unable to generate an action potential usually exhibited a low membrane potential (ca -50 mV). These fibres could generate action potentials if they were hyperpolarized using an intracellular current-passing microelectrode. 6. The quantal content of endplate potentials (EPPs) was estimated from the mean EPP and mean MEPP amplitudes in cut muscle fibre preparations. These estimates suggested that quantal content was low at the earliest stages of regeneration, but increased as the muscle fibres matured and became normal at 10-21 days. 7. During repetitive stimulation at 30 Hz there was a fall in the amplitude of EPPs of 40-45%. The fall was similar in regenerating and control fibres. Conducting synapses never exhibited failure to generate an EPP during the period of high-frequency stimulation.

Full text

PDF
405

Images in this article

409Fig. 1
on p.409

Selected References

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

  1. ALLBROOK D. B., AITKEN J. T. Reinnervation of striated muscle after acute ischaemia. J Anat. 1951 Oct;85(4):376–390. [PMC free article] [PubMed] [Google Scholar]
  2. Alnaes E., Rahamimoff R. On the role of mitochondria in transmitter release from motor nerve terminals. J Physiol. 1975 Jun;248(2):285–306. doi: 10.1113/jphysiol.1975.sp010974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BARSTAD J. A. Presynaptic effect of the neuro-muscular transmitter. Experientia. 1962 Dec 15;18:579–580. doi: 10.1007/BF02172193. [DOI] [PubMed] [Google Scholar]
  4. Bennett M. R., Florin T., Woog R. The formation of synapses in regenerating mammalian striated muscle. J Physiol. 1974 Apr;238(1):79–92. doi: 10.1113/jphysiol.1974.sp010511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennett M. R., McLachlan E. M., Taylor R. S. The formation of synapses in reinnervated mammalian striated muscle. J Physiol. 1973 Sep;233(3):481–500. doi: 10.1113/jphysiol.1973.sp010319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bulfield G., Siller W. G., Wight P. A., Moore K. J. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1189–1192. doi: 10.1073/pnas.81.4.1189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlson B. M., Gutmann E. Development of contractile properties of minced muscle regenerates in the rat. Exp Neurol. 1972 Aug;36(2):239–249. doi: 10.1016/0014-4886(72)90020-9. [DOI] [PubMed] [Google Scholar]
  8. Elmqvist D., Quastel D. M. A quantitative study of end-plate potentials in isolated human muscle. J Physiol. 1965 Jun;178(3):505–529. doi: 10.1113/jphysiol.1965.sp007639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Glavinović M. I. Voltage clamping of unparalysed cut rat diaphragm for study of transmitter release. J Physiol. 1979 May;290(2):467–480. doi: 10.1113/jphysiol.1979.sp012784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grubb B. D., Harris J. B. Dye injection confirms the electrophysiological identification of regenerating muscle fibres in the rat. Q J Exp Physiol. 1989 Jul;74(4):541–544. doi: 10.1113/expphysiol.1989.sp003301. [DOI] [PubMed] [Google Scholar]
  11. Harris J. B., Cullen M. J. Muscle necrosis caused by snake venoms and toxins. Electron Microsc Rev. 1990;3(2):183–211. doi: 10.1016/0892-0354(90)90001-9. [DOI] [PubMed] [Google Scholar]
  12. Harris J. B., Johnson M. A. Further observations on the pathological responses of rat skeletal muscle to toxins isolated from the venom of the Australian tiger snake, Notechis scutatus scutatus. Clin Exp Pharmacol Physiol. 1978 Nov-Dec;5(6):587–600. doi: 10.1111/j.1440-1681.1978.tb00714.x. [DOI] [PubMed] [Google Scholar]
  13. Harris J. B., Maltin C. A. Myotoxic activity of the crude venom and the principal neurotoxin, taipoxin, of the Australian taipan, Oxyuranus scutellatus. Br J Pharmacol. 1982 May;76(1):61–75. doi: 10.1111/j.1476-5381.1982.tb09191.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harris J. B., Pollard S. L. Neuromuscular transmission in the murine mutants "motor end-plate disease" and "jolting". J Neurol Sci. 1986 Dec;76(2-3):239–253. doi: 10.1016/0022-510x(86)90172-3. [DOI] [PubMed] [Google Scholar]
  15. Harris J. B., Ribchester R. R. The relationship between end-plate size and transmitter release in normal and dystrophic muscles of the mouse. J Physiol. 1979 Nov;296:245–265. doi: 10.1113/jphysiol.1979.sp013003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hennig R., Lømo T. Firing patterns of motor units in normal rats. Nature. 1985 Mar 14;314(6007):164–166. doi: 10.1038/314164a0. [DOI] [PubMed] [Google Scholar]
  17. Jirmanová I., Thesleff S. Ultrastructural study of experimental muscle degeneration and regeneration in the adult rat. Z Zellforsch Mikrosk Anat. 1972;131(1):77–97. doi: 10.1007/BF00307202. [DOI] [PubMed] [Google Scholar]
  18. Karlsson E., Eaker D., Rydén L. Purification of a presynaptic neurotoxin from the venom of the australian tiger snake Notechis scutatus scutatus. Toxicon. 1972 Jun;10(4):405–413. doi: 10.1016/0041-0101(72)90066-9. [DOI] [PubMed] [Google Scholar]
  19. Kelly S. S. The effect of age on neuromuscular transmission. J Physiol. 1978 Jan;274:51–62. doi: 10.1113/jphysiol.1978.sp012133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kuno M., Turkanis S. A., Weakly J. N. Correlation between nerve terminal size and transmitter release at the neuromuscular junction of the frog. J Physiol. 1971 Mar;213(3):545–556. doi: 10.1113/jphysiol.1971.sp009399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LILEY A. W. The effects of presynaptic polarization on the spontaneous activity at the mammalian neuromuscular junction. J Physiol. 1956 Nov 28;134(2):427–443. doi: 10.1113/jphysiol.1956.sp005655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MARTIN A. R. A further study of the statistical composition on the end-plate potential. J Physiol. 1955 Oct 28;130(1):114–122. doi: 10.1113/jphysiol.1955.sp005397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McArdle J. J., Albuquerque E. X. A study of the reinnervation of fast and slow mammalian muscles. J Gen Physiol. 1973 Jan;61(1):1–23. doi: 10.1085/jgp.61.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Morgan J. E., Hoffman E. P., Partridge T. A. Normal myogenic cells from newborn mice restore normal histology to degenerating muscles of the mdx mouse. J Cell Biol. 1990 Dec;111(6 Pt 1):2437–2449. doi: 10.1083/jcb.111.6.2437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Partridge T. A., Sloper J. C. A host contribution to the regeneration of muscle grafts. J Neurol Sci. 1977 Sep;33(3):425–435. doi: 10.1016/0022-510x(77)90138-1. [DOI] [PubMed] [Google Scholar]
  26. Rich M., Lichtman J. W. Motor nerve terminal loss from degenerating muscle fibers. Neuron. 1989 Dec;3(6):677–688. doi: 10.1016/0896-6273(89)90236-5. [DOI] [PubMed] [Google Scholar]
  27. Tonge D. A. Physiological characteristics of re-innervation of skeletal muscle in the mouse. J Physiol. 1974 Aug;241(1):141–153. doi: 10.1113/jphysiol.1974.sp010645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Whalen R. G., Harris J. B., Butler-Browne G. S., Sesodia S. Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev Biol. 1990 Sep;141(1):24–40. doi: 10.1016/0012-1606(90)90099-5. [DOI] [PubMed] [Google Scholar]

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

RESOURCES