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. 1981 Jan;310:57–75. doi: 10.1113/jphysiol.1981.sp013537

The calcium and frequency dependence of the slow inward current 'staircase' in frog atrium.

S Noble, Y Shimoni
PMCID: PMC1274728  PMID: 6785423

Abstract

1. Changes in the magnitude of the slow inward current in the frog atrium were monitored at different stimulation frequencies, using a double sucrose-gap technique. 2. After short rest periods (1.5-3.0 min), repetitive clamp depolarizations applied at frequencies ranging from 0.33 to 1 Hz (20-60/min) resulted in a progressive increase in the slow inward current towards a new level. Action-potential amplitudes and plateau levels usually showed similar increases under these conditions. 3. Changes in the magnitude of the slow inward current were also found when the frequency was changed during constant stimulation. 4. Replacement of calcium ions by strontium or barium ions led to an augmentation or reduction, respectively, of the 'staircase' effect, relative to the effect in calcium-containing solutions. Barium ions were found to greatly increase the slow inward channel 'recovery' time. 5. The results suggest that calcium influx into amphibian atrial fibres contributes to the regulation of the slow inward conductance mechanism. Progressively increasing currents may underlie positive tension staircases.

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Selected References

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  1. Allen D. G., Blinks J. R. Calcium transients in aequorin-injected frog cardiac muscle. Nature. 1978 Jun 15;273(5663):509–513. doi: 10.1038/273509a0. [DOI] [PubMed] [Google Scholar]
  2. Allen D. G., Jewell B. R., Wood E. H. Studies of the contractility of mammalian myocardium at low rates of stimulation. J Physiol. 1976 Jan;254(1):1–17. doi: 10.1113/jphysiol.1976.sp011217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson T. W., Hirsch C., Kavaler F. Mechanism of activation of contraction in frog ventricular muscle. Circ Res. 1977 Oct;41(4):472–480. doi: 10.1161/01.res.41.4.472. [DOI] [PubMed] [Google Scholar]
  4. BLINKS J. R., KOCH-WESER J. Analysis of the effects of changes in rate and rhythm upon myocardial contractility. J Pharmacol Exp Ther. 1961 Dec;134:373–389. [PubMed] [Google Scholar]
  5. Bass B. G. Restitution of the action potential in cat papillary muscle. Am J Physiol. 1975 Jun;228(6):1717–1724. doi: 10.1152/ajplegacy.1975.228.6.1717. [DOI] [PubMed] [Google Scholar]
  6. Bassingthwaighte J. B., Fry C. H., McGuigan J. A. Relationship between internal calcium and outward current in mammalian ventricular muscle; a mechanism for the control of the action potential duration? J Physiol. 1976 Oct;262(1):15–37. doi: 10.1113/jphysiol.1976.sp011583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beeler G. W., Jr, Reuter H. The relation between membrane potential, membrane currents and activation of contraction in ventricular myocardial fibres. J Physiol. 1970 Mar;207(1):211–229. doi: 10.1113/jphysiol.1970.sp009057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boullin D. J. The action of extracellular cations on the release of the sympathetic transmitter from peripheral nerves. J Physiol. 1967 Mar;189(1):85–99. doi: 10.1113/jphysiol.1967.sp008156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Boyett M. R. An analysis of the effect of the rate of stimulation and adrenaline on the duration of the cardiac action potential. Pflugers Arch. 1978 Nov 14;377(2):155–166. doi: 10.1007/BF00582846. [DOI] [PubMed] [Google Scholar]
  10. Boyett M. R., Jewell B. R. A study of the factors responsible for rate-dependent shortening of the action potential in mammalian ventricular muscle. J Physiol. 1978 Dec;285:359–380. doi: 10.1113/jphysiol.1978.sp012576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brown A. M., Orkand R. K. A down then up staircase in frog ventricle due to altered excitation-contraction coupling. J Physiol. 1968 Jul;197(2):295–304. doi: 10.1113/jphysiol.1968.sp008560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brown H. F., Clark A., Noble S. J. Identification of the pace-maker current in frog atrium. J Physiol. 1976 Jul;258(3):521–545. doi: 10.1113/jphysiol.1976.sp011434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brown H. F., McNaughton P. A., Noble D., Noble S. J. Adrenergic control of cardian pacemaker currents. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):527–537. doi: 10.1098/rstb.1975.0029. [DOI] [PubMed] [Google Scholar]
  14. Burn J. H., Gibbons W. R. The release of noradrenaline from sympathetic fibres in relation to calcium concentration. J Physiol. 1965 Nov;181(1):214–223. doi: 10.1113/jphysiol.1965.sp007756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Carmeliet E. Repolarisation and frequency in cardiac cells. J Physiol (Paris) 1977;73(7):903–923. [PubMed] [Google Scholar]
  16. Chapman R. A., Niedergerke R. Interaction between heart rate and calcium concentration in the control of contractile strength of the frog heart. J Physiol. 1970 Dec;211(2):423–443. doi: 10.1113/jphysiol.1970.sp009285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chesnais J. M., Kavaler F., Anderson T. W., Coraboeuf E. Staircase in frog ventricular muscle. Its dependence on membrane excitation and extracellular ionic composition. Circ Res. 1978 Dec;43(6):917–925. doi: 10.1161/01.res.43.6.917. [DOI] [PubMed] [Google Scholar]
  18. Edmands R. E., Greenspan K., Bailey J. C. Role of the premature action potential in contractile potentiation: a study of paired stimulation. Cardiovasc Res. 1972 Jul;6(4):368–374. doi: 10.1093/cvr/6.4.368. [DOI] [PubMed] [Google Scholar]
  19. Einwächter H. M., Haas H. G., Kern R. Membrane current and contraction in frog atrial fibres. J Physiol. 1972 Dec;227(1):141–171. doi: 10.1113/jphysiol.1972.sp010024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  21. Fabiato A., Fabiato F. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol. 1975 Aug;249(3):469–495. doi: 10.1113/jphysiol.1975.sp011026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fozzard H. A. Heart: excitation-contraction coupling. Annu Rev Physiol. 1977;39:201–220. doi: 10.1146/annurev.ph.39.030177.001221. [DOI] [PubMed] [Google Scholar]
  23. GIBBS C. L., JOHNSON E. A. Effect of changes in frequency of stimulation upon rabbit ventricular action potential. Circ Res. 1961 Jan;9:165–170. doi: 10.1161/01.res.9.1.165. [DOI] [PubMed] [Google Scholar]
  24. Gettes L. S., Reuter H. Slow recovery from inactivation of inward currents in mammalian myocardial fibres. J Physiol. 1974 Aug;240(3):703–724. doi: 10.1113/jphysiol.1974.sp010630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gibbons W. R., Fozzard H. A. Slow inward current and contraction of sheep cardiac Purkinje fibers. J Gen Physiol. 1975 Mar;65(3):367–384. doi: 10.1085/jgp.65.3.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Horackova M., Vassort G. Calcium conductance in relation to contractility in frog myocardium. J Physiol. 1976 Aug;259(3):597–616. doi: 10.1113/jphysiol.1976.sp011485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hubbard J. I. Mechanism of transmitter release. Prog Biophys Mol Biol. 1970;21:33–124. [PubMed] [Google Scholar]
  28. Isenberg G. Cardiac Purkinje fibres: [Ca2+]i controls the potassium permeability via the conductance components gK1 and gK2. Pflugers Arch. 1977 Oct 19;371(1-2):77–85. doi: 10.1007/BF00580775. [DOI] [PubMed] [Google Scholar]
  29. Isenberg G. Cardiac Purkinje fibres: the slow inward current component under the influence of modified [Ca2+]i. Pflugers Arch. 1977 Oct 19;371(1-2):61–69. doi: 10.1007/BF00580773. [DOI] [PubMed] [Google Scholar]
  30. Kass R. S., Tsien R. W. Control of action potential duration by calcium ions in cardiac Purkinje fibers. J Gen Physiol. 1976 May;67(5):599–617. doi: 10.1085/jgp.67.5.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lammel E., Niedergerke R., Page S. Analysis of a rapid twitch facilitation in the frog heart. Proc R Soc Lond B Biol Sci. 1975 Jun 17;189(1097):577–590. doi: 10.1098/rspb.1975.0073. [DOI] [PubMed] [Google Scholar]
  32. Léoty C., Alix J. Some technical improvements for the voltage clamp with the double sucrose gap. Pflugers Arch. 1976 Sep 3;365(1):95–97. doi: 10.1007/BF00583633. [DOI] [PubMed] [Google Scholar]
  33. Léoty C., Raymond G. Mechanical activity and ionic currents in frog atrial trabeculae. Pflugers Arch. 1972;334(2):114–128. doi: 10.1007/BF00586785. [DOI] [PubMed] [Google Scholar]
  34. Miller J. P., Wallace A. G., Feezor M. D. A quantitative comparison of the relation between the shape of the action potential and the pattern of stimulation in canine ventricular muscle and Purkinje fibers. J Mol Cell Cardiol. 1971 Mar;2(1):3–19. doi: 10.1016/0022-2828(71)90074-5. [DOI] [PubMed] [Google Scholar]
  35. NIEDERGERKE R. Movements of Ca in beating ventricles of the frog heart. J Physiol. 1963 Jul;167:551–580. doi: 10.1113/jphysiol.1963.sp007167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. NIEDERGERKE R. The staircase phenomenon and the action of calcium on the heart. J Physiol. 1956 Dec 28;134(3):569–583. doi: 10.1113/jphysiol.1956.sp005666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Niedergerke R., Page S. Analysis of catecholamine effects in single atrial trabeculae of the frog heart. Proc R Soc Lond B Biol Sci. 1977 Jun 15;197(1128):333–362. doi: 10.1098/rspb.1977.0074. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Noble S., Shimoni Y. Voltage-dependent potentiation of the slow inward current in frog atrium. J Physiol. 1981 Jan;310:77–95. doi: 10.1113/jphysiol.1981.sp013538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ochi R., Trautwein W. The dependence of cardiac contraction on depolarization and slow inward current. Pflugers Arch. 1971;323(3):187–203. doi: 10.1007/BF00586383. [DOI] [PubMed] [Google Scholar]
  42. Orkand R. K. Facilitation of heart muscle contraction and its dependence on external calcium and sodium. J Physiol. 1968 May;196(2):311–325. doi: 10.1113/jphysiol.1968.sp008509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Reiter M., Stickel F. J. Der Einfluss der Kontraktionsfrequenz auf das Aktionspotential des Meerschweinchem-Papillarmuskels. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol. 1968;260(4):342–365. [PubMed] [Google Scholar]
  45. Reuter H., Scholz H. The regulation of the calcium conductance of cardiac muscle by adrenaline. J Physiol. 1977 Jan;264(1):49–62. doi: 10.1113/jphysiol.1977.sp011657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Reuter H. The dependence of slow inward current in Purkinje fibres on the extracellular calcium-concentration. J Physiol. 1967 Sep;192(2):479–492. doi: 10.1113/jphysiol.1967.sp008310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Reuter H. Time- and voltage-dependent contractile responses in mammalian cardiac muscle. Eur J Cardiol. 1973 Dec;1(2):177–181. [PubMed] [Google Scholar]
  48. Rougier O., Vassort G., Garnier D., Gargouil Y. M., Coraboeuf E. Existence and role of a slow inward current during the frog atrial action potential. Pflugers Arch. 1969;308(2):91–110. doi: 10.1007/BF00587018. [DOI] [PubMed] [Google Scholar]
  49. Sands S. D., Winegrad S. Treppe and total calcium content of the frog ventricle. Am J Physiol. 1970 Mar;218(3):908–910. doi: 10.1152/ajplegacy.1970.218.3.908. [DOI] [PubMed] [Google Scholar]
  50. Siegelbaum S. A., Tsien R. W., Kass R. S. Role of intracellular calcium in the transient outward current of calf Purkinje fibres. Nature. 1977 Oct 13;269(5629):611–613. doi: 10.1038/269611a0. [DOI] [PubMed] [Google Scholar]
  51. Simurda J., Simurdova M., Braveny P., Sumbera J. Slow inward current and action potentials of papillary muscles under non-steady state conditions. Pflugers Arch. 1976 Apr 6;362(3):209–218. doi: 10.1007/BF00581172. [DOI] [PubMed] [Google Scholar]
  52. Spear J. F., Moore E. N. A comparison of alternation in myocardial action potentials and contractility. Am J Physiol. 1971 Jun;220(6):1708–1716. doi: 10.1152/ajplegacy.1971.220.6.1708. [DOI] [PubMed] [Google Scholar]
  53. Trautwein W. The slow inward current in mammalian myocardium. Its relation to contraction. Eur J Cardiol. 1973 Dec;1(2):169–175. [PubMed] [Google Scholar]
  54. Vassort G., Rougier O. Membrane potential and slow inward current dependence of frog cardiac mechanical activity. Pflugers Arch. 1972;331(3):191–203. doi: 10.1007/BF00589126. [DOI] [PubMed] [Google Scholar]

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