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. 1966 Sep 1;50(1):141–169. doi: 10.1085/jgp.50.1.141

Analysis of Depolarizing and Hyperpolarizing Inactivation Responses in Gymnotid Electroplaques

Michael V L Bennett 1, Harry Grundfest 1
PMCID: PMC2225631  PMID: 5971025

Abstract

In electroplaques of several gymnotid fishes hyperpolarizing or depolarizing currents can evoke all-or-none responses that are due to increase in membrane resistance as much as 10- to 12-fold. During a response the emf of the membrane shifts little, if at all, when the cell either is at its normal resting potential, or is depolarized by increasing external K, and in the case of depolarizing responses when either Cl or an impermeant anion is present. Thus, the increase in resistance is due mainly, or perhaps entirely, to decrease in K permeability, termed depolarizing or hyperpolarizing K inactivation, respectively. In voltage clamp measurements the current-voltage relation shows a negative resistance region. This characteristic accounts for the all-or-none initiation and termination of the responses demonstrable in current clamp experiments. Depolarizing inactivation is initiated and reversed too rapidly to measure with present techniques in cells in high K. Both time courses are slowed in cells studied in normal Ringer's. Once established, the high resistance state is maintained as long as an outward current is applied. Hyperpolarizing inactivation occurs in normal Ringer's or with moderate excess K. Its onset is more rapid with stronger stimuli. During prolonged currents it is not maintained; i.e., there is a secondary increase in conductance. Hyperpolarizing inactivation responses exhibit a long refractory period, presumably because of persistence of this secondary increase in conductance.

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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., 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]
  3. BENNETT M. V., GRUNDFEST H. Electrophysiology of electric organ in Gymnotus carapo. J Gen Physiol. 1959 May 20;42(5):1067–1104. doi: 10.1085/jgp.42.5.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. 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]
  7. DODGE F. A., FRANKENHAEUSER B. Membrane currents in isolated frog nerve fibre under voltage clamp conditions. J Physiol. 1958 Aug 29;143(1):76–90. doi: 10.1113/jphysiol.1958.sp006045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. GRUNDFEST H., REUBEN J. P., RICKLES W. H., Jr The electrophysiology and pharmacology of lobster neuromuscular synapses. J Gen Physiol. 1959 Jul 20;42(6):1301–1323. doi: 10.1085/jgp.42.6.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GRUNDFEST H. The mechanisms of discharge of the electric organs in relation to general and comparative electrophysiology. Prog Biophys Biophys Chem. 1957;7:1–85. [PubMed] [Google Scholar]
  12. HAGIWARA S., SAITO N. Voltage-current relations in nerve cell membrane of Onchidium verruculatum. J Physiol. 1959 Oct;148:161–179. doi: 10.1113/jphysiol.1959.sp006279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. MEISSNER H. P. DAS VERHALTEN DER SCHNUERRINGMEMBRAN UNTER DEM EINFLUSS STARKER DEPOLARISIERENDER STROEME. Pflugers Arch Gesamte Physiol Menschen Tiere. 1965 Apr 6;283:213–221. [PubMed] [Google Scholar]
  17. 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]
  18. MUELLER P. Prolonged action potentials from single nodes of Ranvier. J Gen Physiol. 1958 Sep 20;42(1):137–162. doi: 10.1085/jgp.42.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. Nakajima S. Analysis of K inactivation and TEA action in the supramedullary cells of puffer. J Gen Physiol. 1966 Mar;49(4):629–640. doi: 10.1085/jgp.49.4.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nakajima S., Kusano K. Behavior of delayed current under voltage clamp in the supramedullary neurons of puffer. J Gen Physiol. 1966 Mar;49(4):613–628. doi: 10.1085/jgp.49.4.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. OOYAMA H., WRIGHT E. B. Anode break excitation on single Ranvier node of frog nerve. Am J Physiol. 1961 Feb;200:209–218. doi: 10.1152/ajplegacy.1961.200.2.209. [DOI] [PubMed] [Google Scholar]
  26. Ozeki M., Freeman A. R., Grundfest H. The membrane components of crustacean neuromuscular systems. II. Analysis of interactions among the electrogenic components. J Gen Physiol. 1966 Jul;49(6):1335–1349. doi: 10.1085/jgp.0491335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. SEGAL J. R. An anodal threshold phenomenon in the squid giant axon. Nature. 1958 Nov 15;182(4646):1370–1370. doi: 10.1038/1821370a0. [DOI] [PubMed] [Google Scholar]
  30. TASAKI I. Demonstration of two stable states of the nerve membrane in potassium-rich media. J Physiol. 1959 Oct;148:306–331. doi: 10.1113/jphysiol.1959.sp006290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. TASAKI I., KAMIYA N. A STUDY ON ELECTROPHYSIOLOGICAL PROPERTIES OF CARNIVOROUS AMOEBAE. J Cell Physiol. 1964 Jun;63:365–380. doi: 10.1002/jcp.1030630312. [DOI] [PubMed] [Google Scholar]
  32. TOMITA T. A compensation circuit for coaxial and double-barreled microelectrodes. Ire Trans Biomed Electron. 1962 Apr;BME-9:138–141. doi: 10.1109/tbmel.1962.4322979. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. 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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