Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1982 Sep;330:221–242. doi: 10.1113/jphysiol.1982.sp014338

The passive electrical properties of guinea-pig ventricular muscle as examined with a voltage-clamp technique.

J Daut
PMCID: PMC1225295  PMID: 7175743

Abstract

1. A voltage-clamp technique was developed for stable recording of small currents in guinea-pig ventricular muscle. Small cylindrical preparations were impaled with three micro-electrodes, one for measuring the feed-back potential and two for injecting current. 2. The longitudinal potential profile resulting from current injection at one point was measured. It agreed well with the theoretical predictions for a linear cable which is sealed at both ends ('healing over'), with a length constant (lambda) of 580 +/- 145 micron. 3. When the clamp current was injected symmetrically into each half of the preparation via two electronic current pumps a spatially homogeneous clamp could be achieved in preparations with a diameter of less than or equal to 250 micron and a length of less than or equal to 2 lambda. 4. The membrane capacity and the membrane resistance of the preparations at the resting potential were measured with small voltage-clamp pulses. Assuming a specific membrane capacity (Cm) of 1 microF/cm2 a specific membrane resistance (Rm) of 6.7 +/- 1.8 k omega cm2 was obtained in Tyrode solution containing 3 mM-K. 5. The total surface area was calculated from the measured capacity of the preparation assuming a Cm of 1 microF/cm2. The total cellular volume was estimated from optical measurement of the external dimensions of the preparation assuming an extracellular space of 25%. From these data the average surface/volume ratio of individual cells was calculated to be 7200 cm2/cm3. 6. From the measured electrical constants the specific resistance of the intracellular space (Ri) was calculated to be 200-250 omega cm. With small constant current pulses a membrane time constant of 6.6 +/- 1.3 ms was measured. 7. The influence of the extracellular potassium concentration ([K]o) on Rm was studied in the range 1.5-6 mM-[K]o. Rm was found to depend on [K]o less than predicted by the constant field theory.

Full text

PDF
240

Selected References

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

  1. Attwell D., Cohen I. The voltage clamp of multicellular preparations. Prog Biophys Mol Biol. 1977;31(3):201–245. doi: 10.1016/0079-6107(78)90009-3. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Beeler G. W., Jr, Reuter H. Voltage clamp experiments on ventricular myocarial fibres. J Physiol. 1970 Mar;207(1):165–190. doi: 10.1113/jphysiol.1970.sp009055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beeler G. W., McGuigan J. A. Voltage clamping of multicellular myocardial preparations: capabilities and limitations of existing methods. Prog Biophys Mol Biol. 1978;34(3):219–254. doi: 10.1016/0079-6107(79)90019-1. [DOI] [PubMed] [Google Scholar]
  5. Beeler G. W., Reuter H. Reconstruction of the action potential of ventricular myocardial fibres. J Physiol. 1977 Jun;268(1):177–210. doi: 10.1113/jphysiol.1977.sp011853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boyett M. R., Coray A., McGuigan J. A. Cow ventricular muscle. I. The effect of the extracellular potassium concentration on the current-voltage relationship. II. Evidence for a time-dependent outward current. Pflugers Arch. 1980 Dec;389(1):37–44. doi: 10.1007/BF00587926. [DOI] [PubMed] [Google Scholar]
  7. Carmeliet E., Verdonck F. Reduction of potassium permeability by chloride substitution in cardiac cells. J Physiol. 1977 Feb;265(1):193–206. doi: 10.1113/jphysiol.1977.sp011712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chapman R. A., Fry C. H. An analysis of the cable properties of frog ventricular myocardium. J Physiol. 1978 Oct;283:263–282. doi: 10.1113/jphysiol.1978.sp012499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ciani S., Krasne S., Miyazaki S., Hagiwara S. A model for anomalous rectification: electrochemical-potential-dependent gating of membrane channels. J Membr Biol. 1978 Dec 15;44(2):103–134. doi: 10.1007/BF01976035. [DOI] [PubMed] [Google Scholar]
  10. Cleemann L., Morad M. Extracellular potassium accumulation in voltage-clamped frog ventricular muscle. J Physiol. 1979 Jan;286:83–111. doi: 10.1113/jphysiol.1979.sp012608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cleemann L., Morad M. Potassium currents in frog ventricular muscle: evidence from voltage clamp currents and extracellular K accumulation. J Physiol. 1979 Jan;286:113–143. doi: 10.1113/jphysiol.1979.sp012609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clerc L. Directional differences of impulse spread in trabecular muscle from mammalian heart. J Physiol. 1976 Feb;255(2):335–346. doi: 10.1113/jphysiol.1976.sp011283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Colatsky T. J., Tsien R. W. Electrical properties associated with wide intercellular clefts in rabbit Purkinje fibres. J Physiol. 1979 May;290(2):227–252. doi: 10.1113/jphysiol.1979.sp012769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Daut J., Rüdel R. The electrogenic sodium pump in guinea-pig ventricular muscle: inhibition of pump current by cardiac glycosides. J Physiol. 1982 Sep;330:243–264. doi: 10.1113/jphysiol.1982.sp014339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Dreyer F., Peper K. Iontophoretic application of acetylcholine: advantages of high resistance micropipettes in connection with an electronic current pump. Pflugers Arch. 1974 Apr 22;348(3):263–272. doi: 10.1007/BF00587417. [DOI] [PubMed] [Google Scholar]
  19. Dudel J., Peper K., Rüdel R., Trautwein W. Excitatory membrane current in heart muscle (Purkinje fibers). Pflugers Arch Gesamte Physiol Menschen Tiere. 1966;292(3):255–273. doi: 10.1007/BF00362740. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Fozzard H. A., Lee C. O. Influence of changes in external potassium and chloride ions on membrane potential and intracellular potassium ion activity in rabbit ventricular muscle. J Physiol. 1976 Apr;256(3):663–689. doi: 10.1113/jphysiol.1976.sp011345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fray J. C., Laurens N. J. Mechanism by which albumin stimulates renin secretion in isolated kidneys and juxtaglomerular cells. J Physiol. 1981 Nov;320:31–39. doi: 10.1113/jphysiol.1981.sp013932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. GOERKE J., PAGE E. CAT HEART MUSCLE IN VITRO. VI. POTASSIUM EXCHANGE IN PAPILLARY MUSCLES. J Gen Physiol. 1965 May;48:933–948. doi: 10.1085/jgp.48.5.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Hagiwara S., Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18(1):61–80. doi: 10.1007/BF01870103. [DOI] [PubMed] [Google Scholar]
  27. Hagiwara S., Yoshii M. Effects of internal potassium and sodium on the anomalous rectification of the starfish egg as examined by internal perfusion. J Physiol. 1979 Jul;292:251–265. doi: 10.1113/jphysiol.1979.sp012849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hille B., Schwarz W. Potassium channels as multi-ion single-file pores. J Gen Physiol. 1978 Oct;72(4):409–442. doi: 10.1085/jgp.72.4.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Horres C. R., Aiton J. F., Lieberman M. Potassium permeability of embryonic avian heart cells in tissue culture. Am J Physiol. 1979 Mar;236(3):C163–C170. doi: 10.1152/ajpcell.1979.236.3.C163. [DOI] [PubMed] [Google Scholar]
  30. Horres C. R., Lieberman M. Compartmental analysis of potassium efflux from growth-oriented heart cells. J Membr Biol. 1977 Jun 15;34(4):331–350. doi: 10.1007/BF01870307. [DOI] [PubMed] [Google Scholar]
  31. Johnson E. A., Lieberman M. Heart: excitation and contraction. Annu Rev Physiol. 1971;33:479–532. doi: 10.1146/annurev.ph.33.030171.002403. [DOI] [PubMed] [Google Scholar]
  32. Kamiyama A., Matsuda K. Electrophysiological properties of the canine ventricular fiber. Jpn J Physiol. 1966 Aug 15;16(4):407–420. doi: 10.2170/jjphysiol.16.407. [DOI] [PubMed] [Google Scholar]
  33. Kass R. S., Siegelbaum S. A., Tsien R. W. Three-micro-electrode voltage clamp experiments in calf cardiac Purkinje fibres: is slow inward current adequately measured? J Physiol. 1979 May;290(2):201–225. doi: 10.1113/jphysiol.1979.sp012768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. McDonald T. F., Trautwein W. The potassium current underlying delayed rectification in cat ventricular muscle. J Physiol. 1978 Jan;274:217–246. doi: 10.1113/jphysiol.1978.sp012144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McGuigan J. A. Some limitations of the double sucrose gap, and its use in a study of the slow outward current in mammalian ventricular muscle. J Physiol. 1974 Aug;240(3):775–806. doi: 10.1113/jphysiol.1974.sp010634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mirolli M., Talbott S. R. The geometrical factors determining the electrotonic properties of a molluscan neurone. J Physiol. 1972 Dec;227(1):19–34. doi: 10.1113/jphysiol.1972.sp010017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Noma A., Irisawa H. Membrane currents in the rabbit sinoatrial node cell as studied by the double microelectrode method. Pflugers Arch. 1976 Jun 29;364(1):45–52. doi: 10.1007/BF01062910. [DOI] [PubMed] [Google Scholar]
  39. Ohmori H. Inactivation kinetics and steady-state current noise in the anomalous rectifier of tunicate egg cell membranes. J Physiol. 1978 Aug;281:77–99. doi: 10.1113/jphysiol.1978.sp012410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. PAGE E. Cat heart muscle in vitro. III. The extracellular space. J Gen Physiol. 1962 Nov;46:201–213. doi: 10.1085/jgp.46.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Page E. Quantitative ultrastructural analysis in cardiac membrane physiology. Am J Physiol. 1978 Nov;235(5):C147–C158. doi: 10.1152/ajpcell.1978.235.5.C147. [DOI] [PubMed] [Google Scholar]
  42. Reuter H. Properties of two inward membrane currents in the heart. Annu Rev Physiol. 1979;41:413–424. doi: 10.1146/annurev.ph.41.030179.002213. [DOI] [PubMed] [Google Scholar]
  43. Sakamoto Y., Goto M. A study of the membrane constants in the dog myocardium. Jpn J Physiol. 1970 Feb 15;20(1):30–41. doi: 10.2170/jjphysiol.20.30. [DOI] [PubMed] [Google Scholar]
  44. Sakamoto Y. Membrane characteristics of the canine papillary muscle fiber. J Gen Physiol. 1969 Dec;54(6):765–781. doi: 10.1085/jgp.54.6.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sommer J. R., Johnson E. A. Cardiac muscle. A comparative study of Purkinje fibers and ventricular fibers. J Cell Biol. 1968 Mar;36(3):497–526. doi: 10.1083/jcb.36.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Tanaka I., Sasaki Y. On the electrotonic spread in cardiac muscle of the mouse. J Gen Physiol. 1966 Jul;49(6):1089–1110. doi: 10.1085/jgp.0491089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tille J. Electrotonic interaction between muscle fibers in the rabbit ventricle. J Gen Physiol. 1966 Sep;50(1):189–202. doi: 10.1085/jgp.50.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Trautwein W., McDonald T. F. Current-voltage relations in ventricular muscle preparations from different species. Pflugers Arch. 1978 Apr 25;374(1):79–89. doi: 10.1007/BF00585700. [DOI] [PubMed] [Google Scholar]
  49. Vaughan-Jones R. D. Non-passive chloride distribution in mammalian heart muscle: micro-electrode measurement of the intracellular chloride activity. J Physiol. 1979 Oct;295:83–109. doi: 10.1113/jphysiol.1979.sp012956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Vaughan-Jones R. D. Regulation of chloride in quiescent sheep-heart Purkinje fibres studied using intracellular chloride and pH-sensitive micro-electrodes. J Physiol. 1979 Oct;295:111–137. doi: 10.1113/jphysiol.1979.sp012957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. WEIDMANN S. The electrical constants of Purkinje fibres. J Physiol. 1952 Nov;118(3):348–360. doi: 10.1113/jphysiol.1952.sp004799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Weidmann S. Electrical constants of trabecular muscle from mammalian heart. J Physiol. 1970 Nov;210(4):1041–1054. doi: 10.1113/jphysiol.1970.sp009256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Weidmann S. The diffusion of radiopotassium across intercalated disks of mammalian cardiac muscle. J Physiol. 1966 Nov;187(2):323–342. doi: 10.1113/jphysiol.1966.sp008092. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES