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. 1965 Nov 1;49(2):321–349. doi: 10.1085/jgp.49.2.321

Analysis of Spike Electrogenesis and Depolarizing K Inactivation in Electroplaques of Electrophorus electricus, L

Yutaka Nakamura 1, Shigehiro Nakajima 1, Harry Grundfest 1
PMCID: PMC2195482  PMID: 19873566

Abstract

Voltage clamp analyses, combined with pharmacological tools demonstrate the independence of reactive Na and K channels in electrically excitable membrane of eel electroplaques. Spike electrogenesis is due to Na activation and is eliminated by tetrodotoxin or mussel poison, or by substituting choline, K, Cs, or Rb for Na in the medium. The K channels remain reactive, but K activation is always absent, the electroplaques responding only with K inactivation. This is indicated by an increased resistance when the membrane is depolarized by more than about 30 mv. The resting resistance (1 to 5 ohm cm2) is dependent upon the ionic conditions, but when K inactivation occurs the resistance becomes about 10 ohm cm2 in all conditions. K inactivation does not change the EMF significantly. The transition from low to high resistance may give rise to a negative-slope voltage current characteristic, and to regenerative inactivation responses under current clamp. The further demonstration that pharmacological K inactivation (by Cs or Rb) leaves Na activation and spike electrogenesis unaffected emphasizes the independence of the reactive processes and suggests different chemical compositions for the membrane structures through which they operate.

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Selected References

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  1. ADRIAN R. H. Potassium chloride movement and the membrane potential of frog muscle. J Physiol. 1960 Apr;151:154–185. [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. ALTAMIRANO M., COATES C. W. Effect of potassium on electroplax of Electrophorus electricus. J Cell Physiol. 1957 Feb;49(1):69–101. doi: 10.1002/jcp.1030490105. [DOI] [PubMed] [Google Scholar]
  4. ALTAMIRANO M., COATES C. W., GRUNDFEST H. Mechanisms of direct and neural excitability in electroplaques of electric eel. J Gen Physiol. 1955 Jan 20;38(3):319–360. doi: 10.1085/jgp.38.3.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. ALTAMIRANO M., COATES C. W., GRUNDFEST H., NACHMANSOHN D. Electrical activity in electric tissue. III. Modifications of electrical activity by acetylcholine and related compounds. Biochim Biophys Acta. 1955 Apr;16(4):449–463. doi: 10.1016/0006-3002(55)90263-8. [DOI] [PubMed] [Google Scholar]
  6. ALTAMIRANO M., COATES C. W., GRUNDFEST H., NACHMANSOHN D. Mechanisms of bioelectric activity in electric tissue. I. The response to indirect and direct stimulation of electroplaques of Electrophorus electricus. J Gen Physiol. 1953 Sep;37(1):91–110. doi: 10.1085/jgp.37.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. ALTAMIRANO M. Electrical properties of the innervated membrane of the electroplax of electric eel. J Cell Physiol. 1955 Oct;46(2):249–277. doi: 10.1002/jcp.1030460205. [DOI] [PubMed] [Google Scholar]
  8. Adrian R. H., Freygang W. H. The potassium and chloride conductance of frog muscle membrane. J Physiol. 1962 Aug;163(1):61–103. doi: 10.1113/jphysiol.1962.sp006959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. CARMELIET E. E. Chloride ions and the membrane potential of Purkinje fibres. J Physiol. 1961 Apr;156:375–388. doi: 10.1113/jphysiol.1961.sp006682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. CARR C. W., SOLLNER K. THE ELECTROOSMOTIC EFFECTS ARISING FROM THE INTERACTION OF THE SELECTIVELY ANION AND SELECTIVELY CATION PERMEABLE PARTS OF MOSAIC MEMBRANES. Biophys J. 1964 May;4:189–201. doi: 10.1016/s0006-3495(64)86777-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DECK K. A., KERN R., TRAUTWEIN W. VOLTAGE CLAMP TECHNIQUE IN MAMMALIAN CARDIAC FIBRES. Pflugers Arch Gesamte Physiol Menschen Tiere. 1964 Jun 9;280:50–62. doi: 10.1007/BF00412615. [DOI] [PubMed] [Google Scholar]
  12. DECK K. A., TRAUTWEIN W. IONIC CURRENTS IN CARDIAC EXCITATION. Pflugers Arch Gesamte Physiol Menschen Tiere. 1964 Jun 9;280:63–80. doi: 10.1007/BF00412616. [DOI] [PubMed] [Google Scholar]
  13. FINKELSTEIN A. ELECTRICAL EXCITABILITY OF ISOLATED FROG SKIN AND TOAD BLADDER. J Gen Physiol. 1964 Jan;47:545–565. doi: 10.1085/jgp.47.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Finkelstein A., Mauro A. Equivalent Circuits as Related to Ionic Systems. Biophys J. 1963 May;3(3):215–237. doi: 10.1016/s0006-3495(63)86817-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GRUNDFEST H. Ionic mechanisms in electrogenesis. Ann N Y Acad Sci. 1961 Sep 6;94:405–457. doi: 10.1111/j.1749-6632.1961.tb35554.x. [DOI] [PubMed] [Google Scholar]
  16. HALL A. E., HUTTER O. F., NOBLE D. Current-voltage relations of Purkinje fibres in sodium-deficient solutions. J Physiol. 1963 Apr;166:225–240. doi: 10.1113/jphysiol.1963.sp007102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. KEYNES R. D., MARTINS-FERREIRA H. Membrane potentials in the electroplates of the electric eel. J Physiol. 1953 Feb 27;119(2-3):315–351. doi: 10.1113/jphysiol.1953.sp004849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. MOORE J. W. Excitation of the squid axon membrane in isosmotic potassium chloride. Nature. 1959 Jan 24;183(4656):265–266. doi: 10.1038/183265b0. [DOI] [PubMed] [Google Scholar]
  22. Müller-Mohnssen H., Balk O. Relations between stationary and dynamic properties of Ranvier nodes. Nature. 1965 Sep 18;207(5003):1255–1257. doi: 10.1038/2071255a0. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. NAKAMURA Y., NAKAJIMA S., GRUNDFEST H. EEL ELECTROPLAQUES: SPIKE ELECTROGENESIS WITHOUT POTASSIUM ACTIVATION. Science. 1964 Oct 9;146(3641):266–268. doi: 10.1126/science.146.3641.266. [DOI] [PubMed] [Google Scholar]
  25. NARAHASHI T., DEGUCHI T., URAKAWA N., OHKUBO Y. Stabilization and rectification of muscle fiber membrane by tetrodotoxin. Am J Physiol. 1960 May;198:934–938. doi: 10.1152/ajplegacy.1960.198.5.934. [DOI] [PubMed] [Google Scholar]
  26. NARAHASHI T., MOORE J. W., SCOTT W. R. TETRODOTOXIN BLOCKAGE OF SODIUM CONDUCTANCE INCREASE IN LOBSTER GIANT AXONS. J Gen Physiol. 1964 May;47:965–974. doi: 10.1085/jgp.47.5.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nakamura Y., Nakajima S., Grundfest H. The action of tetrodotoxin on electrogenic components of squid giant axons. J Gen Physiol. 1965 Jul;48(6):975–996. [PubMed] [Google Scholar]
  28. REUBEN J. P., GAINER H. Membrance conductance during depolarizing postsynaptic potentials of crayfish muscle fibres. Nature. 1962 Jan 13;193:142–143. doi: 10.1038/193142a0. [DOI] [PubMed] [Google Scholar]
  29. REUBEN J. P., WERMAN R., GRUNDFEST H. The ionic mechanisms of hyperpolarizing responses in lobster muscle fibers. J Gen Physiol. 1961 Nov;45:243–265. doi: 10.1085/jgp.45.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. SCHANTZ E. J. Biochemical studies on paralytic shellfish poisons. Ann N Y Acad Sci. 1960 Nov 17;90:843–855. doi: 10.1111/j.1749-6632.1960.tb26427.x. [DOI] [PubMed] [Google Scholar]
  31. TASAKI I., FREYGANG W. H., Jr The parallelism between the action potential, action current, and membrane resistance at a node of Ranvier. J Gen Physiol. 1955 Nov 20;39(2):211–223. doi: 10.1085/jgp.39.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. WEIDMANN S. Effect of current flow on the membrane potential of cardiac muscle. J Physiol. 1951 Oct 29;115(2):227–236. doi: 10.1113/jphysiol.1951.sp004667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. WERMAN R., GRUNDFEST H. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol. 1961 May;44:997–1027. doi: 10.1085/jgp.44.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]

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