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. 1976 Dec;263(2):215–238. doi: 10.1113/jphysiol.1976.sp011629

An evaluation of the membrane constants and the potassium conductance in metabolically exhausted muscle fibres.

R Fink, H C Lüttgau
PMCID: PMC1307698  PMID: 1087932

Abstract

1. The membrane characteristics of metabolically poisoned and mechanically exhausted frog skeletal muscle fibres were investigated with intracellular micro-electrodes. 2. When cyanide plus iodoacetate were applied as metabolic poisons twitch tension declined towards zero after 150-300 stimuli (0-3 Hz; temperature = 0 degrees C). At the beginning of stimulation the mean resting potenial fell from -75 to -69 mV; it rose subsequently to -83 mV. The membrane resistance decreased during this stimulation period along a sigmoid time course to 4-6% of the original value. 3. In completely exhausted fibres the following membrane constants were estimated (23 degrees C): length constant, 0-31 mm; input resistance, 31 komega; membrane resistance, 58 omega.cm2. These values were calculated under the assumption of a constant internal resistivity of 170 omega. cm. The Q10 values of these constants were similar to those in normal fibres. Afew experiments revealed that the membrane capacity remained roughly constant under these conditions. 4. The current-voltage relation of exhausted fibres was approximately linear in the range between -60 and -100 mV. At less negative potentials the conductance increased slightly while at more negative potentials it decreased. The latter, in particular, became more evident when the imput current was converted into membrane current density by applying Cole's theorem. 5TEA+ and Rb+ in the external solution increased the membrane resistance of exhausted fibres by more than one order of magnitude. The major part of the membrane conductance induced by exhaustion, however, could not be blocked by these ions or Zn2+. 6. Chloride-free test solutions were used to measure the relative contributions of potassium and chloride ions to the membrane conductance. The relation GK:GC1 changed from 2:3 in normal fibres to 5:1 in exhausted ones. In absolute terms GK rose from ca. 130 to 14,300 mumho/cm2 and GC1 from ca. 200 to 2900 mumho/cm2. The discrimination between K+ and Na+ by the resting membrane in exhausted fibres was probably equal to or even higher than that under normal conditions. 7. In normal fibres the input resistance decreased by up to 20% after the external application of 1-2 mM caffeine, which is known to release calcium ions from internal stores. The elevation in internal Ca2+ by direct injection caused a small and, as a rule, irreversible decrease in input resistance which was probably partly due to local damage to the surface membrane. 8. It is concluded that in metabolically exhausted muscle fibres the surface and tubular membranes are still intact and that the observed decrease in membrane resistance is mainly due to an increase in potassium conductance. In addition, the results indicate that the gating mechanism of the potassium channels (presumably those with the characteristics of the slow component) is affected when energy reserves diminish.

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Selected References

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

  1. ADRIAN R. H. THE RUBIDIUM AND POTASSIUM PERMEABILITY OF FROG MUSCLE MEMBRANE. J Physiol. 1964 Dec;175:134–159. doi: 10.1113/jphysiol.1964.sp007508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. ADRIAN R. H. The effect of internal and external potassium concentration on the membrane potential of frog muscle. J Physiol. 1956 Sep 27;133(3):631–658. doi: 10.1113/jphysiol.1956.sp005615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. AXELSSON J., THESLEFF S. Activation of the contractile mechanism in striated muscle. Acta Physiol Scand. 1958 Oct 28;44(1):55–66. doi: 10.1111/j.1748-1716.1958.tb01608.x. [DOI] [PubMed] [Google Scholar]
  4. Adrian R. H., Chandler W. K., Hodgkin A. L. Slow changes in potassium permeability in skeletal muscle. J Physiol. 1970 Jul;208(3):645–668. doi: 10.1113/jphysiol.1970.sp009140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Adrian R. H., Slayman C. L. Membrane potential and conductance during transport of sodium, potassium and rubidium in frog muscle. J Physiol. 1966 Jun;184(4):970–1014. doi: 10.1113/jphysiol.1966.sp007961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Almers W. Potassium conductance changes in skeletal muscle and the potassium concentration in the transverse tubules. J Physiol. 1972 Aug;225(1):33–56. doi: 10.1113/jphysiol.1972.sp009928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Almers W. The decline of potassium permeability during extreme hyperpolarization in frog skeletal muscle. J Physiol. 1972 Aug;225(1):57–83. doi: 10.1113/jphysiol.1972.sp009929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. COLE K. S. Non-linear current-potential relations in an axon membrane. J Gen Physiol. 1961 Jul;44:1055–1057. doi: 10.1085/jgp.44.6.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eisenberg R. S., Gage P. W. Ionic conductances of the surface and transverse tubular membranes of frog sartorius fibers. J Gen Physiol. 1969 Mar;53(3):279–297. doi: 10.1085/jgp.53.3.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FATT P., KATZ B. An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol. 1951 Nov 28;115(3):320–370. doi: 10.1113/jphysiol.1951.sp004675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gage P. W., Eisenberg R. S. Action potentials, afterpotentials, and excitation-contraction coupling in frog sartorius fibers without transverse tubules. J Gen Physiol. 1969 Mar;53(3):298–310. doi: 10.1085/jgp.53.3.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grabowski W., Lobsiger E. A., Lüttgau H. C. The effect of repetitive stimulation at low frequencies upon the electrical and mechanical activity of single muscle fibres. Pflugers Arch. 1972;334(3):222–239. doi: 10.1007/BF00626225. [DOI] [PubMed] [Google Scholar]
  13. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hodgkin A. L., Nakajima S. Analysis of the membrane capacity in frog muscle. J Physiol. 1972 Feb;221(1):121–136. doi: 10.1113/jphysiol.1972.sp009743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hodgkin A. L., Nakajima S. The effect of diameter on the electrical constants of frog skeletal muscle fibres. J Physiol. 1972 Feb;221(1):105–120. doi: 10.1113/jphysiol.1972.sp009742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hutter O. F., Warner A. E. Action of some foreign cations and anions on the chloride permeability of frog muscle. J Physiol. 1967 Apr;189(3):445–460. doi: 10.1113/jphysiol.1967.sp008178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hutter O. F., Warner A. E. The pH sensitivity of the chloride conductance of frog skeletal muscle. J Physiol. 1967 Apr;189(3):403–425. doi: 10.1113/jphysiol.1967.sp008176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lüttgau H. C., Oetliker H. The action of caffeine on the activation of the contractile mechanism in straited muscle fibres. J Physiol. 1968 Jan;194(1):51–74. doi: 10.1113/jphysiol.1968.sp008394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meech R. W. Intracellular calcium injection causes increased potassium conductance in Aplysia nerve cells. Comp Biochem Physiol A Comp Physiol. 1972 Jun 1;42(2):493–499. doi: 10.1016/0300-9629(72)90128-4. [DOI] [PubMed] [Google Scholar]
  20. Meech R. W. The sensitivity of Helix aspersa neurones to injected calcium ions. J Physiol. 1974 Mar;237(2):259–277. doi: 10.1113/jphysiol.1974.sp010481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. NAKAJIMA S., IWASAKI S., OBATA K. Delayed rectification and anomalous rectification in frog's skeletal muscle membrane. J Gen Physiol. 1962 Sep;46:97–115. doi: 10.1085/jgp.46.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stanfield P. R. The differential effects of tetraethylammonium and zinc ions on the resting conductance of frog skeletal muscle. J Physiol. 1970 Jul;209(1):231–256. doi: 10.1113/jphysiol.1970.sp009164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stanfield P. R. The effect of the tetraethylammonium ion on the delayed currents of frog skeletal muscle. J Physiol. 1970 Jul;209(1):209–229. doi: 10.1113/jphysiol.1970.sp009163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stefani E., Schmidt H. A convenient method for repeated intracellular recording of action potentials from the same muscle fibre without membrane damage. Pflugers Arch. 1972;334(3):276–278. doi: 10.1007/BF00626229. [DOI] [PubMed] [Google Scholar]
  25. Weber A., Herz R. The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol. 1968 Nov;52(5):750–759. doi: 10.1085/jgp.52.5.750. [DOI] [PMC free article] [PubMed] [Google Scholar]

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