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. 1979 Dec;297:135–162. doi: 10.1113/jphysiol.1979.sp013032

Measurement and significance of the reversal potential for the pace-maker current (iK2) in sheep Purkinje fibres.

D DiFrancesco, M Ohba, C Ojeda
PMCID: PMC1458712  PMID: 536907

Abstract

1. The apparent reversal potential (Erev) of the pace-maker current (iK2) is found to depend on the experimental protocol used for its measurement. Evidence is presented showing that depolarizing (hyperpolarizing) pulses given before a test hyperpolarization used to determine Erev, shift Erev to more negative (positive) values. These shifts are opposite to those expected if the only effect of pre-pulses were to change the concentration of potassium in extracellular clefts ([K]c) via accumulation and depletion processes. 2. This effect is shown to be due to the fact that Erev is dependent on s0, the degree of activation of iK2 at the start of the test hyperpolarization. 3. When a suitable protocol is used, depletion of cleft K can be demonstrated to take place during a large hyperpolarization. Changes in the level of [K]c induced by pre-pulses must therefore also affect the Erev determination. 4. A simplified three-compartment model has been used to investigate how K accumulation and depletion can affect the time course of iK2, with particular reference to the problem of Erev determination. Computed examples show that the model is able to reproduce the main features of the time course of iK2 recorded near its reversal potential and the changes induced by pre-pulses on Erev measuremnet. By contrast, simulation on a linear cable model rules out the possibility that such results are due to voltage non-uniformity. 5. The three-compartment model predicts that the measured value of Erev differs from EK2 for two reasons: (1) when the recorded current trace is flat iK2 is still outward and decaying, and (2) the K equilibrium potential shifts to more negative values while the test hyperpolarization is applied. 6. The finding that Erev is directly affected by changes in s at the beginning of the test pulse is discussed in relation to the action of agents (such as Ca2+, H+, salicylate, adrenaline and ouabain) which are found to shift both the s00 curve and Erev.

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Selected References

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

  1. 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]
  2. 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]
  3. Aronson R. S., Gelles J. M. The effect of ouabain, dinitrophenol, and lithium on the pacemaker current in sheep cardiac Purkinje fibers. Circ Res. 1977 May;40(5):517–524. doi: 10.1161/01.res.40.5.517. [DOI] [PubMed] [Google Scholar]
  4. Baumgarten C. M., Isenberg G. Depletion and accumulation of potassium in the extracellular clefts of cardiac Purkinje fibers during voltage clamp hyperpolarization and depolarization. Pflugers Arch. 1977 Mar 11;368(1-2):19–31. doi: 10.1007/BF01063450. [DOI] [PubMed] [Google Scholar]
  5. Baumgarten C. M., Isenberg G., McDonald T. F., Ten Eick R. E. Depletion and accumulation of potassium in the extracellular clefts of cardiac Purkinje fibers during voltage clamp hyperpolarization and depolarization: experiments in sodium-free bathing media. J Gen Physiol. 1977 Aug;70(2):149–169. doi: 10.1085/jgp.70.2.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown H. F., Noble D., Noble S. J. The influence of non-uniformity on the analysis of potassium currents in heart muscle. J Physiol. 1976 Jul;258(3):615–629. doi: 10.1113/jphysiol.1976.sp011437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown R. H., Jr, Cohen I., Noble D. The interactions of protons, calcium and potassium ions on cardiac Purkinje fibres. J Physiol. 1978 Sep;282:345–352. doi: 10.1113/jphysiol.1978.sp012467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown R. H., Jr, Noble D. Displacement of activator thresholds in cardiac muscle by protons and calcium ions. J Physiol. 1978 Sep;282:333–343. doi: 10.1113/jphysiol.1978.sp012466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cohen I., Daut J., Noble D. An analysis of the actions of low concentrations of ouabain on membrane currents in Purkinje fibres. J Physiol. 1976 Aug;260(1):75–103. doi: 10.1113/jphysiol.1976.sp011505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cohen I., Daut J., Noble D. The effects of potassium and temperature on the pace-maker current, iK2, in Purkinje fibres. J Physiol. 1976 Aug;260(1):55–74. doi: 10.1113/jphysiol.1976.sp011504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cohen I., Eisner D., Noble D. The action of adrenaline on pace-maker activity in cardiac Purkinje fibres. J Physiol. 1978 Jul;280:155–168. doi: 10.1113/jphysiol.1978.sp012378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cohen I., Noble D., Ohba M., Ojeda C. Action of salicylate ions on the electrical properties of sheep cardiac Purkinje fibres. J Physiol. 1979 Dec;297(0):163–185. doi: 10.1113/jphysiol.1979.sp013033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cohen I., Noble D., Ohba M., Ojeda C. The interaction of ouabain and salicylate on sheep cardiac muscle. J Physiol. 1979 Dec;297(0):187–205. doi: 10.1113/jphysiol.1979.sp013034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. DiFrancesco D., McNaughton P. A. The effects of calcium on outward membrane currents in the cardiac Purkinje fibre. J Physiol. 1979 Apr;289:347–373. doi: 10.1113/jphysiol.1979.sp012741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DiFrancesco D., Ohba M. Dependence of the apparent reversal potential for the pace-maker current iK2 on its degree of activation in cardiac Purkinje fibres [proceedings]. J Physiol. 1978 Jul;280:73P–74P. [PubMed] [Google Scholar]
  17. Dubois J. M., Bergman C. Potassium accumulation in the perinodal space of frog myelinated axons. Pflugers Arch. 1975 Jul 21;358(2):111–124. doi: 10.1007/BF00583922. [DOI] [PubMed] [Google Scholar]
  18. Dudel J., Peper K., Rüdel R., Trautwein W. The potassium component of membrane current in Purkinje fibers. Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;296(4):308–327. doi: 10.1007/BF00362531. [DOI] [PubMed] [Google Scholar]
  19. FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Hauswirth O., Noble D., Tsien R. W. Adrenaline: mechanism of action on the pacemaker potential in cardiac Purkinje fibers. Science. 1968 Nov 22;162(3856):916–917. doi: 10.1126/science.162.3856.916. [DOI] [PubMed] [Google Scholar]
  22. Hellam D. C., Studt J. W. A core-conductor model of the cardiac Purkinje fibre based on structural analysis. J Physiol. 1974 Dec;243(3):637–660. doi: 10.1113/jphysiol.1974.sp010770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Isenberg G. Cardiac Purkinje fibres: [Ca2+]i controls steady state potassium conductance. Pflugers Arch. 1977 Oct 19;371(1-2):71–76. doi: 10.1007/BF00580774. [DOI] [PubMed] [Google Scholar]
  24. Isenberg G., Trautwein W. The effect of dihydro-ouabain and lithium-ions on the outward current in cardiac Purkinje fibers. Evidence for electrogenicity of active transport. Pflugers Arch. 1974;350(1):41–54. doi: 10.1007/BF00586737. [DOI] [PubMed] [Google Scholar]
  25. Kline R., Morad M. Potassium efflux and accumulation in heart muscle. Evidence from K +/- electrode experiments. Biophys J. 1976 Apr;16(4):367–372. doi: 10.1016/S0006-3495(76)85694-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maughan D. W. Some effects of prolonged polarization on membrane currents in bullfrog atrial muscle. J Membr Biol. 1973;11(4):331–352. doi: 10.1007/BF01869829. [DOI] [PubMed] [Google Scholar]
  27. McAllister R. E., Noble D. The time and voltage dependence of the slow outward current in cardiac Purkinje fibres. J Physiol. 1966 Oct;186(3):632–662. doi: 10.1113/jphysiol.1966.sp008060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McAllister R. E., Noble D., Tsien R. W. Reconstruction of the electrical activity of cardiac Purkinje fibres. J Physiol. 1975 Sep;251(1):1–59. doi: 10.1113/jphysiol.1975.sp011080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Noble D., Stein R. B. The threshold conditions for initiation of action potentials by excitable cells. J Physiol. 1966 Nov;187(1):129–162. doi: 10.1113/jphysiol.1966.sp008079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Noble D., Tsien R. W. The kinetics and rectifier properties of the slow potassium current in cardiac Purkinje fibres. J Physiol. 1968 Mar;195(1):185–214. doi: 10.1113/jphysiol.1968.sp008454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Noble S. J. Potassium accumulation and depletion in frog atrial muscle. J Physiol. 1976 Jul;258(3):579–613. doi: 10.1113/jphysiol.1976.sp011436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Peper K., Trautwein W. A note on the pacemaker current in Purkinje fibers. Pflugers Arch. 1969 Jun 19;309(4):356–361. doi: 10.1007/BF00587758. [DOI] [PubMed] [Google Scholar]
  33. Rogus E. M., Cheng L. C., Zierler K. beta-Adrenergic effect on Na+-K+ transport in rat skeletal muscle. Biochim Biophys Acta. 1977 Jan 21;464(2):347–355. doi: 10.1016/0005-2736(77)90009-8. [DOI] [PubMed] [Google Scholar]
  34. Tsien R. W. Effects of epinephrine on the pacemaker potassium current of cardiac Purkinje fibers. J Gen Physiol. 1974 Sep;64(3):293–319. doi: 10.1085/jgp.64.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. VASSALLE M. CARDIAC PACEMAKER POTENTIALS AT DIFFERENT EXTRA-AND INTRACELLULAR K CONCENTRATIONS. Am J Physiol. 1965 Apr;208:770–775. doi: 10.1152/ajplegacy.1965.208.4.770. [DOI] [PubMed] [Google Scholar]

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