Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1980 Jun 1;75(6):655–672. doi: 10.1085/jgp.75.6.655

Action potentials in fast- and slow-twitch mammalian muscles during reinnervation and development

PMCID: PMC2215269  PMID: 7391811

Abstract

Action potentials (APs) were recorded from the extrajunctional membrane of surface fibers of the fast-twitch extensor digitorum longus (extensor) and the slow-twitch soleus muscles of adult rats. APs of the extensor muscle had a significantly faster rate of rise and fall, as well as a shorter duration, than those of the soleus. In addition, the overshoot of APs and the resting membrane potential was greater for the extensor. Whereas the soleus produced only one AP regardless of the stimulus duration, the number of extensor responses was directly proportional to the stimulus duration. This repetitive activity was greatly reduced by a concentration of tetrodotoxin (TTX) as low as 5 X 10(11) g/ml. Within 8 d after crush of the nerves to these two muscles, all differences in AP properties disappeared and both muscles became partially resistant to TTX. Reinnervation brought about a redifferentiation so that differences in AP were again significant at 22 d after nerve crush. However, the rate of rise of extensor APs did not attain normal values even as late as 60 d after nerve crush. APs were found to be the same for extensor and soleus muscles from 12-d-old rats. At 18 d after birth, rate of rise was equivalent to that of adult muscle for the soleus although 50--60 d were required before this parameter was fully mature for the extensor. Nevertheless, APs of the extensor and soleus were clearly differentiated within 25 d after birth. Differences in fast and slow muscle APs are discussed with regard to differences in ion gradients and sarcolemmal conductance.

Full Text

The Full Text of this article is available as a PDF (880.0 KB).

Selected References

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

  1. Adrian R. H., Marshall M. W. Sodium currents in mammalian muscle. J Physiol. 1977 Jun;268(1):223–250. doi: 10.1113/jphysiol.1977.sp011855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albuquerque E. X., McIsaac R. J. Fast and slow mammalian muscles after denervation. Exp Neurol. 1970 Jan;26(1):183–202. doi: 10.1016/0014-4886(70)90099-3. [DOI] [PubMed] [Google Scholar]
  3. Close R. Dynamic properties of fast and slow skeletal muscles of the rat after nerve cross-union. J Physiol. 1969 Oct;204(2):331–346. doi: 10.1113/jphysiol.1969.sp008916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Colquhoun D., Rang H. P., Ritchie J. M. The binding of tetrodotoxin and alpha-bungarotoxin to normal and denervated mammalian muscle. J Physiol. 1974 Jul;240(1):199–226. doi: 10.1113/jphysiol.1974.sp010607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Duval A., Léoty C. Ionic currents in mammalian fast skeletal muscle. J Physiol. 1978 May;278:403–423. doi: 10.1113/jphysiol.1978.sp012312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. ECCLES J. C., ECCLES R. M., LUNDBERG A. The action potentials of the alpha motoneurones supplying fast and slow muscles. J Physiol. 1958 Jul 14;142(2):275–291. doi: 10.1113/jphysiol.1958.sp006015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ellisman M. H., Rash J. E., Staehelin L. A., Porter K. R. Studies of excitable membranes. II. A comparison of specializations at neuromuscular junctions and nonjunctional sarcolemmas of mammalian fast and slow twitch muscle fibers. J Cell Biol. 1976 Mar;68(3):752–774. doi: 10.1083/jcb.68.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ellisman M. H., Rash J. E. Studies of excitable membranes. III. Freeze-fracture examination of the membrane specializations at the neuromuscular junction and in the non-junctional sarcolemma after denervation. Brain Res. 1977 Dec 2;137(2):197–206. doi: 10.1016/0006-8993(77)90333-x. [DOI] [PubMed] [Google Scholar]
  9. Gage P. W., McBurney R. N., Schneider G. T. Effects of some aliphatic alcohols on the conductance change caused by a quantum of acetylcholine at the toad end-plate. J Physiol. 1975 Jan;244(2):409–429. doi: 10.1113/jphysiol.1975.sp010806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. HODGKIN A. L., HUXLEY A. F., KATZ B. Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol. 1952 Apr;116(4):424–448. doi: 10.1113/jphysiol.1952.sp004716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harris J. B., Marshall M. W. Tetrodotoxin-resistant action potentials in newborn rat muscle. Nat New Biol. 1973 Jun 6;243(127):191–192. doi: 10.1038/newbio243191a0. [DOI] [PubMed] [Google Scholar]
  12. Hoh J. F., Salafsky B. Effects of nerve cross-union on rat intracellular potassium in fast-twitch and slow-twitch rat muscles. J Physiol. 1971 Jul;216(1):171–179. doi: 10.1113/jphysiol.1971.sp009516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Huizar P., Kuno M., Miyata Y. Differentiation of motoneurones and skeletal muscles in kittens. J Physiol. 1975 Nov;252(2):465–479. doi: 10.1113/jphysiol.1975.sp011152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. JENERICK H. PHASE PLANE TRAJECTORIES OF THE MUSCLE SPIKE POTENTIAL. Biophys J. 1963 Sep;3:363–377. doi: 10.1016/s0006-3495(63)86827-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. McArdle J. J., Garnes R. C., Sellin L. C. Membrane electrical properties of fast- and slow-twitch muscles from rats with experimental hyperthyroidism. Exp Neurol. 1977 Jul;56(1):168–178. doi: 10.1016/0014-4886(77)90147-9. [DOI] [PubMed] [Google Scholar]
  16. McArdle J. J., Sansone F. M. Re-innervation of fast and slow twitch muscle following nerve crush at birth. J Physiol. 1977 Oct;271(3):567–586. doi: 10.1113/jphysiol.1977.sp012015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mommaerts W. F., Seraydarian K., Suh M., Kean C. J., Buller A. J. The conversion of some biochemical properties of mammalian skeletal muscles following cross-reinnervation. Exp Neurol. 1977 Jun;55(3 Pt 1):637–653. doi: 10.1016/0014-4886(77)90290-4. [DOI] [PubMed] [Google Scholar]
  18. Redfern P., Thesleff S. Action potential generation in denervated rat skeletal muscle. I. Quantitative aspects. Acta Physiol Scand. 1971 Apr;81(4):557–564. doi: 10.1111/j.1748-1716.1971.tb04932.x. [DOI] [PubMed] [Google Scholar]
  19. SRETER F. A., WOO G. CELL WATER, SODIUM, AND POTASSIUM IN RED AND WHITE MAMMALIAN MUSCLES. Am J Physiol. 1963 Dec;205:1290–1294. doi: 10.1152/ajplegacy.1963.205.6.1290. [DOI] [PubMed] [Google Scholar]
  20. Sellin L. C., McArdle J. J. Colchicine blocks neurotrophic regulation of the resting membrane potential in reinnervating skeletal muscle. Exp Neurol. 1977 May;55(2):483–492. doi: 10.1016/0014-4886(77)90016-4. [DOI] [PubMed] [Google Scholar]
  21. Thesleff S., Vyskocil F., Ward M. R. The action potential in end-plate and extrajunctional regions of rat skeletal muscle. Acta Physiol Scand. 1974 Jun;91(2):196–202. doi: 10.1111/j.1748-1716.1974.tb05676.x. [DOI] [PubMed] [Google Scholar]
  22. Valdiosera R., Clausen C., Eisenberg R. S. Impedance of frog skeletal muscle fibers in various solutions. J Gen Physiol. 1974 Apr;63(4):460–491. doi: 10.1085/jgp.63.4.460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Vyskocil F. Action potentials of the rat diaphragm and their sensitivity to tetrodotoxin during postnatal development and old age. Pflugers Arch. 1974;352(2):155–163. doi: 10.1007/BF00587514. [DOI] [PubMed] [Google Scholar]
  24. Walton M., Fozzard H. A. The relation of Vmax to INa, GNa, and h infinity in a model of the cardiac Purkinje fiber. Biophys J. 1979 Mar;25(3):407–420. doi: 10.1016/S0006-3495(79)85312-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Westgaard R. H. Influence of activity on the passive electrical properties of denervated soleus muscle fibres in the rat. J Physiol. 1975 Oct;251(3):683–697. doi: 10.1113/jphysiol.1975.sp011116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yonemura K. Resting and action potentials in red and white muscles of the rat. Jpn J Physiol. 1967 Dec 15;17(6):708–719. doi: 10.2170/jjphysiol.17.708. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES