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. 1975 Apr 1;65(4):527–550. doi: 10.1085/jgp.65.4.527

A synthetic strand of cardiac muscle: its passive electrical properties

M Lieberman, T Sawanobori, JM Kootsey, EA Johnson
PMCID: PMC2214931  PMID: 1097581

Abstract

The passive electrical properties of synthetic strands of cardiac muscle, grown in tissue culture, were studied using two intracellular microelectrodes: one to inject a rectangular pulse of current and the other to record the resultant displacement of membrane potential at various distances from the current source. In all preparations, the potential displacement, instead of approaching a steady value as would be expected for a cell with constant electrical properties, increased slowly with time throughout the current step. In such circumstances, the specific electrical constants for the membrane and cytoplasm must not be obtained by applying the usual methods, which are based on the analytical solution of the partial differential equation describing a one-dimensional cell with constant electrical properties. A satisfactory fit of the potential waveforms was, however, obtained with numerical solutions of a modified form of this equation in which the membrane resistance increased linearly with time. Best fits of the waveforms from 12 preparations gave the following values for the membrane resistance times unit length, membrane capacitance per unit length, and for the myoplasmic resistance: 1.22 plus or minus 0.13 x 10-5 omegacm, 0.224 plus or minus 0.023 uF with cm-minus 1, and 1.37 plus or minus 0.13 x 10-7 omegacm-minus 1, respectively. The value of membrane capacitance per unit length was close to that obtained from the time constant of the foot of the action potential and was in keeping with the generally satisfactory fit of the recorded waveforms with solutions of the cable equation in which the membrane impedance is that of a single capacitor and resistor in parallel. The area of membrane per unit length and the cross-sectional area of myoplasm at any given length of the preparation were determined from light and composite electron micrographs, and these were used to calculate the following values for the specific electrical membrane resistance, membrane capacitance, and the resistivity of the cytoplasm: 20.5 plus or minus 3.0 x 10-3 omegacm-2, l.54 plus or minus 0.24 uFWITHcm-minus 2, and 180 plus or minus 34 omegacm, respectively.

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Selected References

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  1. Adrian R. H., Peachey L. D. The membrane capacity of frog twitch and slow muscle fibres. J Physiol. 1965 Nov;181(2):324–336. doi: 10.1113/jphysiol.1965.sp007764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BURROWS R., LAMB J. F. Sodium and potassium fluxes in cells cultured from chick embryo heart muscle. J Physiol. 1962 Aug;162:510–531. doi: 10.1113/jphysiol.1962.sp006947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berkinelit M. B., Kovalev S. A., Smolianinov V. V., Chailakhian L. M. Opredelenie osnovnykh élektricheskikh kharakteristik miokarda zheludochka liagushki. Biofizika. 1965;10(5):861–867. [PubMed] [Google Scholar]
  4. Bonke F. I. Electronic spread in the sinoatrial node of the rabbit heart. Pflugers Arch. 1973 Mar 5;339(1):17–23. doi: 10.1007/BF00586978. [DOI] [PubMed] [Google Scholar]
  5. DeHaan R. L., Gottlieb S. H. The electrical activity of embryonic chick heart cells isolated in tissue culture singly or in interconnected cell sheets. J Gen Physiol. 1968 Oct;52(4):643–665. doi: 10.1085/jgp.52.4.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dulhunty A. F., Gage P. W. Electrical properties of toad sartorius muscle fibres in summer and winter. J Physiol. 1973 May;230(3):619–641. doi: 10.1113/jphysiol.1973.sp010208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fischbach G. D., Nameroff M., Nelson P. G. Electrical properties of chick skeletal muscle fibers developing in cell culture. J Cell Physiol. 1971 Oct;78(2):289–299. doi: 10.1002/jcp.1040780218. [DOI] [PubMed] [Google Scholar]
  8. Freygang W. H., Trautwein W. The structural implications of the linear electrical properties of cardiac Purkinje strands. J Gen Physiol. 1970 Apr;55(4):524–547. doi: 10.1085/jgp.55.4.524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. GEORGE E. P. Resistance values in a syncytium. Aust J Exp Biol Med Sci. 1961 Jun;39:267–274. doi: 10.1038/icb.1961.27. [DOI] [PubMed] [Google Scholar]
  10. Gage P. W., Eisenberg R. S. Action potentials, afterpotentials, and excitation-contraction coupling in frog sartorius fibers without transverse tubules. J Gen Physiol. 1969 Mar;53(3):298–310. doi: 10.1085/jgp.53.3.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gage P. W., Eisenberg R. S. Capacitance of the surface and transverse tubular membrane of frog sartorius muscle fibers. J Gen Physiol. 1969 Mar;53(3):265–278. doi: 10.1085/jgp.53.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HARSCH M., GREEN J. W. ELECTROLYTE ANALYSES OF CHICK EMBRYONIC FLUIDS AND HEART TISSUES. J Cell Physiol. 1963 Dec;62:319–326. doi: 10.1002/jcp.1030620312. [DOI] [PubMed] [Google Scholar]
  13. Hirakow R. Ultrastructural characteristics of the mammalian and sauropsidan heart. Am J Cardiol. 1970 Feb;25(2):195–203. doi: 10.1016/0002-9149(70)90579-5. [DOI] [PubMed] [Google Scholar]
  14. Hyde A., Blondel B., Matter A., Cheneval J. P., Filloux B., Girardier L. Homo- and heterocellular junctions in cell cultures: an electrophysiological and morphological study. Prog Brain Res. 1969;31:283–311. doi: 10.1016/S0079-6123(08)63247-1. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Johnson E. A., Sommer J. R. A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J Cell Biol. 1967 Apr;33(1):103–129. doi: 10.1083/jcb.33.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kootsey J. M., Johnson E. A. Buffer amplifier with femtofarad input capacity using operational amplifiers. IEEE Trans Biomed Eng. 1973 Sep;20(5):389–391. doi: 10.1109/TBME.1973.324240. [DOI] [PubMed] [Google Scholar]
  18. Lieberman M. Effects of cell density and low K on action potentials of cultured chick heart cells. Circ Res. 1967 Dec;21(6):879–888. doi: 10.1161/01.res.21.6.879. [DOI] [PubMed] [Google Scholar]
  19. Lieberman M. Electrophysiological studies of a synthetic strand of cardiac muscle. Physiologist. 1973 Nov;16(4):551–563. [PubMed] [Google Scholar]
  20. Lieberman M., Manasek F. J., Sawanobori T., Johnson E. A. Cytochalasin B: its morphological and electrophysiological actions on synthetic strands of cardiac muscle. Dev Biol. 1973 Apr;31(2):380–403. doi: 10.1016/0012-1606(73)90273-x. [DOI] [PubMed] [Google Scholar]
  21. Lieberman M., Roggeveen A. E., Purdy J. E., Johnson E. A. Synthetic strands of cardiac muscle: growth and physiological implication. Science. 1972 Feb 25;175(4024):909–911. doi: 10.1126/science.175.4024.909. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. McDonald T. F., DeHaan R. L. Ion levels and membrane potential in chick heart tissue and cultured cells. J Gen Physiol. 1973 Jan;61(1):89–109. doi: 10.1085/jgp.61.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mobley B. A., Page E. The surface area of sheep cardiac Purkinje fibres. J Physiol. 1972 Feb;220(3):547–563. doi: 10.1113/jphysiol.1972.sp009722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. 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]
  28. Pappano A. J., Sperelakis N. Low K+ conductance and low resting potentials of isolated single cultured heart cells. Am J Physiol. 1969 Oct;217(4):1076–1082. doi: 10.1152/ajplegacy.1969.217.4.1076. [DOI] [PubMed] [Google Scholar]
  29. Purdy J. E., Liebeman M., Roggeveen A. E., Kirk R. G. Synthetic strands of cardiac muscle. Formation and ultrastructure. J Cell Biol. 1972 Dec;55(3):563–578. doi: 10.1083/jcb.55.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. SPERELAKIS N., LEHMKUHL D. EFFECT OF CURRENT ON TRANSMEMBRANE POTENTIALS IN CULTURED CHICK HEART CELLS. J Gen Physiol. 1964 May;47:895–927. doi: 10.1085/jgp.47.5.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Schanne O. F., De Ceretti E. R. Measurement of input impedance and cytoplasmic resistivity with a single microelectrode. Can J Physiol Pharmacol. 1971 Jul;49(7):713–716. doi: 10.1139/y71-096. [DOI] [PubMed] [Google Scholar]
  33. Schanne O., Kawata H., Schäfer B., Lavallée M. A study on the electrical resistance of the frog sartorius muscle. J Gen Physiol. 1966 May;49(5):897–912. doi: 10.1085/jgp.49.5.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shiba H., Kanno Y. Further study of the two-dimensional cable theory: an electric model for a flat thin association of cells with a directional intercellular communication. Biophysik. 1971;7(4):295–301. doi: 10.1007/BF01190241. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Sommer J. R., Johnson E. A. Cardiac muscle. A comparative ultrastructural study with special reference to frog and chicken hearts. Z Zellforsch Mikrosk Anat. 1969;98(3):437–468. [PubMed] [Google Scholar]
  37. TRAUTWEIN W., KASSEBAUM D. G. On the mechanism of spontaneous impulse generation in the pacemaker of the heart. J Gen Physiol. 1961 Nov;45:317–330. doi: 10.1085/jgp.45.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Tomita T. Membrane capacity and resistance of mammalian smooth muscle. J Theor Biol. 1966 Nov;12(2):216–227. doi: 10.1016/0022-5193(66)90114-7. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Valdiosera R., Clausen C., Eisenberg R. S. Circuit models of the passive electrical properties of frog skeletal muscle fibers. J Gen Physiol. 1974 Apr;63(4):432–459. doi: 10.1085/jgp.63.4.432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]

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