Summary
The passive electrical properties of neonatal rat heart cells grown in monolayer cultures were determined. Hyperpolarizing current pulses were injected through one microelectrode via an active bridge circuit. Membrane voltage displacements caused by the injected current pulses were measured at various distances from the first with a second microelectrode. Using a modified least-squares method the experimental results were fitted to a Bessel function, which is the steady-state solution of the differential equation describing the relation between membrane voltage caused by current injection and interelectrode distance in a very large and very thin plane cell. Best fit was obtained with a space constant of 360 μm and an internal resistivity of 500 Ω cm. From these figures, specific membrane resistance was calculated to be 1,300 Ω cm2, assuming all current to leave through the upper surface of the monolayer.
The time constant of the membrane was measured from the time course of the current-induced membrane voltage displacements. From its value of 1.7 msec a membrane capacity of 1.3 μF/cm2 was calculated.
From these results and some literature data on nexus distribution (A. W. Spira,J. Ultrastruct. Res. 34:409, 1971) specific nexus resistance was calculated to range between 0.25 and 1.25 Ω cm2, depending on the amount of folding of the intercalated discs. The results suggest that spread of activation in monolayer cultures of heart cells by means of local circuit currents is very likely.
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References
Abramowitz, M., Stegun, I. A. 1964. Handbook of Mathematical Functions. National Bureau of Standards, Washington, D. C.
Azarnia, R., Loewenstein, W. R. 1971. Intercellular communication and tissue growth. V. A cancer cell strain that fails to make permeable membrane junctions with normal cells.J. Membrane Biol. 6:368.
Barr, L., Dewey, M. M., Berger, W. 1965. Propagation of action potentials and the structure of the nexus in cardiac muscle.J. Gen. Physiol. 48:797.
Cedergren, B., Harary, I. 1964. In vitro studies on single beating rat heart cells. VII. Ultrastructure of the beating cell layer.J. Ultrastruct. Res. 11:443.
Couch, R. J., West, T. C., Hoff, H. E. 1969. Development of the action potential of the prenatal rat heart.Circulation Res. 24:19.
Eisenberg, R. S., Johnson, E. A. 1970. Three dimensional electrical field problems in physiology.In: Progress in Biophysics and Molecular Biology. J. A. V. Butler and D. Noble, editors. Vol. 20, p. 1 Pergamon Press, Oxford.
Frank, K., Fuortes, M. G. F. V. 1956. Stimulation of spinal motoneurons with intracellular microelectrodes.J. Physiol. 134:451.
George, E. P. 1961. Resistance values in a syncytium.Aust. J. Exp. Biol. Sci. 39:267.
Goshima, K. 1970. Formation of nexuses and electrotonic transmission between myocardial and FL cells in monolayer culture.Exp. Cell Res. 63:124.
Harary, I., Farley, B.. 1963. In vitro studies on single beating rat heart cells. I. Growth and Organisation.Exp. Cell Res. 29:451.
Heppner, D. B., Plonsey, R. 1970. Simulation of interaction of cardiac cells.Biophys. J. 10:1057.
Hyde, A., Blondel, B., Matter, A., Cheneval, J. P., Filloux, B., Girardier, L. 1969. Homo and heterocellular junctions in cell cultures: An electrophysiological and morphological study.In: Progress in Brain Research. K. Akert and P. G. Waser, editors. Vol. 31, p. 283. Elsevier Publishing Co., Amsterdam.
Jongsma, H. J., Hollander, C. C. 1971. Synchronisation of cardiac pacemaker cells.Pflüg. Arch. Ges. Physiol. 328:263.
Kloot, W. G. van der, Dane, B. 1964. Conduction of the action potential in the frog ventricle.Science 146:74.
Lehmkuhl, D., Sperelakis, N. 1963. Transmembrane potentials of trypsin-dispersed chick heart cells cultured in vitro.Amer. J. Physiol. 205:1213.
Lehmkuhl, D., Sperelakis, N. 1965. Electrotonic spread in cultured chick heart cells.J. Cell. Comp. Physiol. 66:119.
Loewenstein, W. R., Kanno, Y. 1964. Studies on an epithelial (gland) cell junction. I. Modifications of surface membrane permeability.J. Cell Biol. 22:565.
Loewenstein, W. R., Socolar, S. J., Higashino, S., Kanno, Y., Davidson, H. 1965. Intercellular communication: Renal, uninary bladder, sensory and salivary gland cells.Science 149:295.
Marcus, P. I., Cieciura, S. J., Puck, T. T. 1956. Clonal growth in vitro of epithelial cells from normal human tissues.J. Exp. Med. 104:615.
Noble, D. 1962. The voltage dependence of the cardiac membrane conductance.Biophys. J. 2:381.
Pager, J., Bernard, C., Gargouil, Y. M. 1965. Evolution au cours de la croissance foetale de effets de l'actylcholine au niveau de l'oreillette de rat.Compt. Rend. Soc. Biol. 159:2470.
Politoff, A. L., Socolar, S. J., Loewenstein, W. R. 1969. Permeability of a cell membrane junction. Dependence on energy metabolism.J. Gen. Physiol. 53:498.
Sakamoto, Y., Goto, M. 1970. A study of the membrane constants in the dog myocardium.Jap. J. Physiol. 20:30.
Schanne, O. 1969. Measurement of cytoplasmatic resistivity by means of the glass microelectrode.In: Glass Microelectrodes. M. Lavallee, O. F. Schanne, and N. C. Hebert, editors. p. 299. John Wiley and Sons, Inc., New York.
Shiba, H. 1971. Heavyside's “Bessel cable” for flat simple epithelial cells with low resistive junctional membranes.J. Theoret. Biol. 30:59.
Siegenbeek van Heukelom, J. 1971. Cell communication in epithelial systems. Ph. D. Thesis. University of Utrecht, The Netherlands, and Bronder-Offset, Rotterdam.
Sjöstrand, F. S., Anderson, E. 1954. Electron microscopy of the intercalated disks of cardiac muscle tissue.Experientia 10:369.
Sperelakis, N. 1969. Lack of electrical coupling between contiguous myocardial cells in vertebrate hearts.In: Comparative Physiology of the Heart: Current Trends. F. W. McCann, editor. p. 135. Birkhauser, Basel.
Sperelakis, N., Hoshiko, T., Berne, R. M. 1960. Nonsyncytial nature of cardiac muscle: Membrane resistance of single cells.Amer. J. Physiol. 198:531.
Sperelakis, N., Lehmkuhl, D. 1964. Effect of current on transmembrane potentials in cultured chick heart cells.J. Gen. Physiol. 47:895.
Spira, A. W. 1971. The nexus in the intercalated disk of the canine heart: Quantitative data for an estimation of its resistance.J. Ultrastruct. Res. 34:409.
Tanaka, I., Sasaki, Y. 1966. The electrotonic spread in cardiac muscle of the mouse.J. Gen. Physiol. 49:1089.
Tille, J. 1966. Electrotonic interaction between muscle fibers in the rabbit ventricle.J. Gen. Physiol. 50:189.
Trautwein, W., Kuffler, S. W., Edwards, C. 1956. Changes in membrane characteristics of heart muscle during inhibition.J. Gen. Physiol. 40:135.
Weidmann, S. 1952. The electrical constants of Purkinje fibres.J. Physiol. 118:348.
Weidmann, S. 1966. Diffusion of radiopotassium across intercalated disks of mammalian cardiac muscle.J. Physiol. 187:323.
Weidmann, S. 1970. Electrical constants of trabecular muscle from mammalian heart.J. Physiol. 210:1041.
Wollenberger, A. 1964. Rhythmic and arrhythmic contractile activity of single myocardial cells cultured in vitro.Circulation Res. (Suppl. II), XIV–XI:184.
Woodbury, J. W. 1962. Cellular electrophysiology of the heartIn: Handbook of Physiology. W. F. Hamilton, editor. Sect. 2, Circulation I, p. 237, American Physiological Society, Washington, D. C.
Woodbury, J. W., Crill, W. E. 1961. On the problem of impulse conduction in the atrium.In: Nervous Inhibition. E. Florey, editor. p. 124. Pergamon Press, Oxford.
Woodbury, J. W., Crill, W. E. 1970. The potential in the gap between two abutting cardiac muscle cells.Biophys. J. 10:1076.
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Jongsma, H.J., van Rijn, H.E. Electrotonic spread of current in monolayer cultures of neonatal rat heart cells. J. Membrain Biol. 9, 341–360 (1972). https://doi.org/10.1007/BF01868061
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DOI: https://doi.org/10.1007/BF01868061