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. 1978 Jul;280:537–558. doi: 10.1113/jphysiol.1978.sp012400

Potassium efflux in heart muscle during activity: extracellular accumulation and its implications.

R P Kline, M Morad
PMCID: PMC1282675  PMID: 308540

Abstract

1. Extracellular K+ activity and transmembrane potential were simultaneously monitored with a K+-selective micro-electrode placed in the extracellular space and a standard KCl-filled micro-electrode in the intracellular space of the frog ventricular muscle. 2. K+ was found to accumulate during activity and had the approximate magnitude and time course to account for the measured membrane depolarization. 3. The magnitude of the K+ accumulation depended on the frequency of stimulation, diameter of the muscle and temperature of the bathing solution. 4. The time constants of accumulation and decay were dependent only on the diameter and the temperature of the strip. A Q10 of 2 was measured for the decay of accumulated K+. 5. Double barrelled K+-electrodes were used to monitor the change in K+ activity accompanying a single action potential, since the reference barrel allowed for rapid compensation of the electrical potential fluctuations encountered in the subendothelial space. 6. K+ accumulated continuously during the plateau to a level which increased external K concentration by about 1 mM. This increase in the subendothelial space corresponds to about 1-3 muA/cm2 or 10-30 pmole/cm2-sec-1 of net K+ efflux. These values are at least an order of magnitude larger than required to discharge the membrane capacitance. 7. There is no direct relation between action potential duration and rate of development or magnitude of K+ accumulation during that action potential. 8. Increase in the external K concentration, while shortening the action potential and depolarizing the membrane, does not lead to an increased rate of accumulation of K+. The presence of Ni2+, on the other hand, prolongs the action potential and decreases the rate of K+ accumulation. 9. The results suggest that there is a substantial and continuous efflux of K+ during the action potential, which sums during rapid beating, resulting in membrane depolarization and alteration of action potential duration. The change in action potential duration in response to rate may be caused by alteration of EK in the local micro-environments.

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Selected References

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  1. Babskii E. B., Donskikh E. A. Elektrofiziologicheskoe issledovanie deistviia ionov nikelia na miokard. Dokl Akad Nauk SSSR. 1968 Jan-Feb;178(1):248–251. [PubMed] [Google Scholar]
  2. CARMELIET E., LACQUET L. Durée du potentiel d'action ventriculaire de grenouille en fonction de la fréquence; influence des variations ioniques de potassium et sodium. Arch Int Physiol Biochim. 1958 Feb;66(1):1–21. doi: 10.3109/13813455809085118. [DOI] [PubMed] [Google Scholar]
  3. Chapman R. A., Niedergerke R. Effects of calcium on the contraction of the hypodynamic frog heart. J Physiol. 1970 Dec;211(2):389–421. doi: 10.1113/jphysiol.1970.sp009284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cleemann L., Morad M. Extracellular potassium accumulation and inward-going potassium rectification in voltage clamped ventricular muscle. Science. 1976 Jan 9;191(4222):90–92. doi: 10.1126/science.1246599. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Goldman Y., Morad M. Ionic membrane conductance during the time course of the cardiac action potential. J Physiol. 1977 Jul;268(3):655–695. doi: 10.1113/jphysiol.1977.sp011876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goldman Y., Morad M. Measurement of transmembrane potential and current in cardiac muscle: a new voltage clamp method. J Physiol. 1977 Jul;268(3):613–654. doi: 10.1113/jphysiol.1977.sp011875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Kunze D. L. Rate-dependent changes in extracellular potassium in the rabbit atrium. Circ Res. 1977 Jul;41(1):122–127. doi: 10.1161/01.res.41.1.122. [DOI] [PubMed] [Google Scholar]
  10. Lamb J. F., McGuigan J. A. The efflux of potassium, sodium, chloride, calcium and sulphate ions and of sorbitol and glycerol during the cardiac cycle in frog's ventricle. J Physiol. 1968 Mar;195(2):283–315. doi: 10.1113/jphysiol.1968.sp008459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Langer G. A. Ion fluxes in cardiac excitation and contraction and their relation to myocardial contractility. Physiol Rev. 1968 Oct;48(4):708–757. doi: 10.1152/physrev.1968.48.4.708. [DOI] [PubMed] [Google Scholar]
  12. Lebovitz R. M. A theoretical examination of ionic interactions between neural and non-neural membranes. Biophys J. 1970 May;10(5):423–444. doi: 10.1016/S0006-3495(70)86310-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lux H. D., Neher E. The equilibration time course of (K + ) 0 in cat cortex. Exp Brain Res. 1973 Apr 30;17(2):190–205. doi: 10.1007/BF00235028. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Morad M., Orkand R. K. Excitation-concentration coupling in frog ventricle: evidence from voltage clamp studies. J Physiol. 1971 Dec;219(1):167–189. doi: 10.1113/jphysiol.1971.sp009656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Neher E., Lux H. D. Rapid changes of potassium concentration at the outer surface of exposed single neurons during membrane current flow. J Gen Physiol. 1973 Mar;61(3):385–399. doi: 10.1085/jgp.61.3.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Niedergerke R., Orkand R. K. The dual effect of calcium on the action potential of the frog's heart. J Physiol. 1966 May;184(2):291–311. doi: 10.1113/jphysiol.1966.sp007916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Orkand R. K., Nicholls J. G., Kuffler S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):788–806. doi: 10.1152/jn.1966.29.4.788. [DOI] [PubMed] [Google Scholar]
  20. Page S. G., Niedergerke R. Structures of physiological interest in the frog heart ventricle. J Cell Sci. 1972 Jul;11(1):179–203. doi: 10.1242/jcs.11.1.179. [DOI] [PubMed] [Google Scholar]
  21. Sandblom J., Eisenman G., Walker J. L., Jr Electrical phenomena associated with the transport of ions and ion pairs in liquid ion-exchange membranes. I. Zero current properties. J Phys Chem. 1967 Nov;71(12):3862–3870. doi: 10.1021/j100871a022. [DOI] [PubMed] [Google Scholar]
  22. Sandlbom J., Eisenman G., Walker J. L., Jr Electrical phenomena associated with the transport of ions and ion pairs in liquid ion-exchange membranes. II. Nonzero current properties. J Phys Chem. 1967 Nov;71(12):3871–3878. doi: 10.1021/j100871a023. [DOI] [PubMed] [Google Scholar]
  23. Staley N. A., Benson E. S. The ultrastructure of frog ventricular cardiac muscle and its relationship to mechanism of excitation-contraction coupling. J Cell Biol. 1968 Jul;38(1):99–114. doi: 10.1083/jcb.38.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. WEIDMANN S. Shortening of the cardiac action potential due to a brief injection of KCl following the onset of activity. J Physiol. 1956 Apr 27;132(1):157–163. doi: 10.1113/jphysiol.1956.sp005510. [DOI] [PMC free article] [PubMed] [Google Scholar]

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