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. 1984 Feb 1;83(2):175–192. doi: 10.1085/jgp.83.2.175

Physiological basis of a steady endogenous current in rat lumbrical muscle

PMCID: PMC2215625  PMID: 6325581

Abstract

In an attempt to determine the mechanism by which rat skeletal muscle endplates generate a steady outward current, we measured the effects of several drugs (furosemide, bumetanide, 9-anthracene carboxylic acid [9- AC]) and changes in external ion concentration (Na+, K+, Cl-, Ba++) on resting membrane potential (Vm) and on the steady outward current. Each of the following treatments caused a 10-15-mV hyperpolarization of the membrane: replacement of extracellular Cl- with isethionate, addition of furosemide or bumetanide, and addition of 9-AC. These results suggest that Cl- is actively accumulated by the muscle fibers and that the equilibrium potential of Cl- is more positive than the membrane potential. Removal of external Na+ also caused a large hyperpolarization and is consistent with evidence in other tissues that active Cl- accumulation requires external Na+. The same treatments greatly reduced or abolished the steady outward current, with a time course that paralleled the changes in Vm. These results cannot be explained by a model in which the steady outward current is assumed to arise as a result of a nonuniform distribution of Na+ conductance, but they are consistent with models in which the steady current is produced by a nonuniform distribution of GCl or GK. Other treatments (Na+-free and K+-free solutions, and 50 microM BaCl2) caused a temporary reversal of the steady current. Parallel measurements of Vm suggested that in none of these cases did the electrochemical driving force for K+ change sign, which makes it unlikely that the steady current arises as a result of a nonuniform distribution of GK. All of the results, however, are consistent with a model in which the steady outward current arises as a result of a nonuniform distribution of Cl- conductance, with GCl lower near the endplate than in extrajunctional regions.

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Selected References

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  1. Aickin C. C., Thomas R. C. An investigation of the ionic mechanism of intracellular pH regulation in mouse soleus muscle fibres. J Physiol. 1977 Dec;273(1):295–316. doi: 10.1113/jphysiol.1977.sp012095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akaike N. Hyperpolarization of mammalian skeletal muscle fibers in K-free media. Am J Physiol. 1982 Jan;242(1):C12–C18. doi: 10.1152/ajpcell.1982.242.1.C12. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Betz W. J., Caldwell J. H. Mapping electric currents around skeletal muscle with a vibrating probe. J Gen Physiol. 1984 Feb;83(2):143–156. doi: 10.1085/jgp.83.2.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bolton T. B., Vaughan-Jones R. D. Continuous direct measurement of intracellular chloride and pH in frog skeletal muscle. J Physiol. 1977 Sep;270(3):801–833. doi: 10.1113/jphysiol.1977.sp011983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caldwell J. H., Betz W. J. Properties of an endogenous steady current in rat muscle. J Gen Physiol. 1984 Feb;83(2):157–173. doi: 10.1085/jgp.83.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dulhunty A. F. Distribution of potassium and chloride permeability over the surface and T-tubule membranes of mammalian skeletal muscle. J Membr Biol. 1979 Apr 9;45(3-4):293–310. doi: 10.1007/BF01869290. [DOI] [PubMed] [Google Scholar]
  8. Dulhunty A. F. The dependence of membrane potential on extracellular chloride concentration in mammalian skeletal muscle fibres. J Physiol. 1978 Mar;276:67–82. doi: 10.1113/jphysiol.1978.sp012220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ellory J. C., Dunham P. B., Logue P. J., Stewart G. W. Anion-dependent cation transport in erythrocytes. Philos Trans R Soc Lond B Biol Sci. 1982 Dec 1;299(1097):483–495. doi: 10.1098/rstb.1982.0146. [DOI] [PubMed] [Google Scholar]
  10. Frizzell R. A., Field M., Schultz S. G. Sodium-coupled chloride transport by epithelial tissues. Am J Physiol. 1979 Jan;236(1):F1–F8. doi: 10.1152/ajprenal.1979.236.1.F1. [DOI] [PubMed] [Google Scholar]
  11. Gadsby D. C., Cranefield P. F. Two levels of resting potential in cardiac Purkinje fibers. J Gen Physiol. 1977 Dec;70(6):725–746. doi: 10.1085/jgp.70.6.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Jaffe L. F., Nuccitelli R. An ultrasensitive vibrating probe for measuring steady extracellular currents. J Cell Biol. 1974 Nov;63(2 Pt 1):614–628. doi: 10.1083/jcb.63.2.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Musch M. W., Orellana S. A., Kimberg L. S., Field M., Halm D. R., Krasny E. J., Jr, Frizzell R. A. Na+-K+-Cl- co-transport in the intestine of a marine teleost. Nature. 1982 Nov 25;300(5890):351–353. doi: 10.1038/300351a0. [DOI] [PubMed] [Google Scholar]
  17. Palade P. T., Barchi R. L. Characteristics of the chloride conductance in muscle fibers of the rat diaphragm. J Gen Physiol. 1977 Mar;69(3):325–342. doi: 10.1085/jgp.69.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Palade P. T., Barchi R. L. On the inhibition of muscle membrane chloride conductance by aromatic carboxylic acids. J Gen Physiol. 1977 Jun;69(6):879–896. doi: 10.1085/jgp.69.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Robbins N. Cation movements in normal and short-term denervated rat fast twitch muscle. J Physiol. 1977 Oct;271(3):605–624. doi: 10.1113/jphysiol.1977.sp012017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Russell J. M. Cation-coupled chloride influx in squid axon. Role of potassium and stoichiometry of the transport process. J Gen Physiol. 1983 Jun;81(6):909–925. doi: 10.1085/jgp.81.6.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Russell J. M. Chloride and sodium influx: a coupled uptake mechanism in the squid giant axon. J Gen Physiol. 1979 Jun;73(6):801–818. doi: 10.1085/jgp.73.6.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sperelakis N., Schneider M. F., Harris E. J. Decreased K+ conductance produced by Ba++ in frog sartorius fibers. J Gen Physiol. 1967 Jul;50(6):1565–1583. doi: 10.1085/jgp.50.6.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Thomas R. C. Membrane current and intracellular sodium changes in a snail neurone during extrusion of injected sodium. J Physiol. 1969 Apr;201(2):495–514. doi: 10.1113/jphysiol.1969.sp008769. [DOI] [PMC free article] [PubMed] [Google Scholar]

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