Summary
A frequency domain equivalent circuit analysis of isolated ventricular cells indicated the presence of an internal membrane structure which has a total capacitance four- to sixfold larger than the surface membrane. The internal membrane was mainly attributed to the sarcoplasmic reticulum since other morphological studies have shown that its area is many-fold larger than that of the surface membrane. Corresponding estimates from the transverse tubular system indicate an area less than that of the surface; thus this structure is not a likely candidate for the observed internal capacitance. Measurements in hypertonic solutions showed that the access resistance to the internal membrane reversibly increased as the tonicity was elevated. Freeze-fractured electron microscopic studies confirmed that hypertonic solutions increased the volume of transverse tubular system, which thus appears to have little relation to the access resistance. The most probable source of the access resistance is the diadic junction to the sarcoplasmic reticulum, which therefore would electrically couple it to the surface membrane.
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References
Attwell, D., Cohen, I. 1977. The voltage clamp of multicellular preparations.Prog. Biophys. Mol. Biol. 31:201–245
Beeler, G.W., McGuigan, J.A.S. 1978. Voltage clamping of multicellular preparations. Capabilities and limitations of existing methods.Prog. Biophys. Mol. Biol. 34:219–254
Bevington, P.R. 1969. Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York
Brown, A.M., Lee, K.S., Powell, T. 1981a. Voltage clamp and internal perfusion of single rat heart muscle cells.J. Physiol. (London) 318:455–477
Brown, A.M., Lee, K.S., Powell, T. 1981b. Sodium current in single rat heart muscle cells.J. Physiol. (London) 318:479–500
Carmeliet, E., Williams, J. 1971. The frequency dependent character of the membrane capacity in cardiac Purkinje fibres.J. Physiol. (London) 213:85–93
Clapham, D.E., DeFelice, L.J. 1982. Small signal impedance of heart cell membranes.J. Membrane Biol. 67:63–71
Dahl, G., Isenberg, G. 1980. Decoupling in heart muscle cells: Correlation with increased cytoplasmic calcium activity and with changes of nexus ultrastructure.J. Membrane Biol. 53:63–75
Deck, K.A., Kern, R., Trautwein, W. 1964. Voltage clamp technique in mammalian cardic fibres.Pfuegers Arch. 280:50–62
Deck, K.A., Trautwein, W. 1964. Ionic currents in cardiac excitation.Pfluegers Arch. 280:63–80
Dow, J.W., Harding, N.G.L., Powell, T. 1981. Isolated cardiac myocytes. I. Preparation of adult myocytes and their homology with intact tissue.Cardiovasc. Res. 15:483–514
Dreyer, F., Peper, K. 1974. Ionophoretic application of acetylcholine: Advantage of high resistance micropipettes in connection with an electronic current pump.Pfluegers Arch. 348:253–272
Dudel, J., Peper, K., Rüdel, R., Trautwein, W. 1966. Excitatory membrane current in heart muscle (Purkinje fibers).Pflueger's Arch. ges. Physiol. 292:255–273
Eisenberg, R.S. 1967. The equivalent circuit of single crab muscle fibers as determined by impedance measurements with intracellular electrodes.J. Gen. Physiol. 53:279–297
Engel, E., Barcilon, V., Eisenberg, R.S. 1972. The interpretation of current voltage relations recorded from a spherical cell with a single microelectrode.Biophys. J. 12:384–403
Falk, G., Fatt, P. 1964. Linear electrical properties of striated muscle fibers observed with intracellular electrodes.Proc. R. Soc. London B 160:69–123
Franzini-Armstrong, C., Heuser, J.E., Rease, T.S., Somlyo, A.P., Somlyo, A.V. 1978. T-tubule swelling in hypertonic solutions: A freeze substitution study.J. Physiol. (London) 283:133–140
Freygang, W.H., Jr., Rapoport, S.I., Peachy, L.D. 1976. Some relations between changes in linear electrical properties of striated muscle and changes in ultrastructure.J. Gen. Physiol. 50:2437–2458
Freygang, W.H., Trautwein, W. 1970. The structural implications of the linear electrical properties of cardiac Purkinje strands.J. Gen. Physiol. 55:524–547
Fozzard, H.A. 1966. Membrane capacity of the cardiac Purkinje fibre.J. Physiol. (London) 182:255–267
Glick, M.R., Burns, A.H., Reddy, W.J. 1974. Dispersion and isolation of beating cells from adult rat heart.Anal. Biochem. 61:32–42
Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.J. 1981. Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches.Pfluegers Arch. 391:85–100
Hellam, D.C., Studt, J.W. 1974. Linear analysis of membrane conductance and capacitance in cardiac Purkinje fibres.J. Physiol. (London) 243:661–694
Hume, J.R., Giles, W. 1981. Active and passive electrical properties of single bullfrog atrial cells.J. Gen. Physiol. 78:19–42
Isenberg, G. 1976. Cardiac Purkinje fibers: Cesium as a tool to block inward rectifying potassium currents.Pfluegers Arch. 356:99–106
Isenberg, G., Kloeckner, U. 1980. Glycocalix is not required for slow inward calcium current in isolated rat heart myocytes.Nature (London) 284:358–360
Isenberg, G., Kloeckner, U. 1982a. Calcium tolerant ventricular myocytes prepared by preincubation in a “KB medium”.Pfluegers Arch. 395:6–18
Isenberg, G., Kloeckner, U. 1982b. Isolated bovine ventricular myocytes, characterization of the action potential.Pfluegers Arch. 395:19–29
Isenberg, G., Kloeckner, U. 1982c. Calcium currents of isolated bovine ventricular myocytes are fast and of large amplitude.Pfluegers Arch. 395:30–41
Isenberg, G., Vereecke, F., Heyden, G. van der, Carmeliet, E. 1983. The shortening of the action potential by DNP in guinea pig ventricular myocytes is mediated by an increase of a time independent K conductance.Pfluegers Arch. 397:251–259
Johnson, E.A., Lieberman, M. 1971. Heart: Excitation and contraction.Annu. Rev. Physiol. 33:479–532
Mathias, R., Ebihara, L., Lieberman, M., Johnson, E.A. 1981. Linear electrical properties of passive and active currents in spherical heart cell clusters.Biophys. J. 36:221–242
Mathias, R.T., Levis, R.A., Eisenberg, R.S. 1980. Electrical models of excitation-contraction coupling and charge movement in skeletal muscle.J. Gen. Physiol. 76:1–33
Moore, L.E., Tsai, T.D. 1983. Ion conductances of the surface and transverse tubular membranes of skeletal muscle.J. Membrane Biol. 73:217–226
Page, E. 1968. Correlations between electron microscopic and physiological observations in heart muscle.J. Gen. Physiol. 51:211s-220s
Page, E. 1978. Quantitative ultrastructural analysis in cardiac membrane physiology.Am. J. Physiol. 235(5):C147-C158
Page, E., Surdyk-Droske, M. 1979. Distribution, surface density, and membrane area of diadic junctional contracts between plasma membrane and terminal cisterns in mammalian ventricle.Circ. Res. 45:260–267
Page, E., Upshaw-Earley, J. 1977. Volume changes in sarcoplasmic reticulum of rat hearts perfused with hypertonic solutions.Circ. Res. 40:355–366
Peskoff, A., Eisenberg, R.S. 1973. Interpretation of some microelectrode measurements of electrical properties of cells.Annu. Rev. Biophys. Bioeng. 2:65–80
Powell, T., Terrar, D.A., Twist, V.W. 1980. Electrical properties of individual cells isolated from the adult rat ventricular myocardium.J. Physiol. (London) 302:131–153
Poussart, D., Moore, L.E., Fishman, H. 1977. Ion movements and kinetics in squid axon. I. Complex admittance.Ann. N.Y. Acad. Sci. 303:355–379
Schneider, M. 1970. Linear electrical properties of the transverse tubules and surface membrane of skeletal muscle fibers.J. Gen. Physiol. 56:640–671
Sommer, J., Johnson, E.A. 1979. The ultrastructure of cardiac muscle.In: Handbook of Physiology. Section 2: Vol 1, pp. 113–186. R.M. Berne, N. Sperelakis, and S.R. Geiger, editors. American Physiological Society, Bethesda
Sommer, J.R., Waugh, R.A. 1976. The ultrastructure of the mammalian cardiac muscle cell—with special emphasis on the tubular-membrane systems.Am. J. Pathol. 82:192–232
Sperelakis, N., Forbes, M.S., Rubio, R. 1974. The tubular systems of myocardial cells: Ultrastructure and possible function.In: Myocardial Biology: Recent Advances in Studies on Cardiac Structure and Metabolism. Vol. 4, pp. 163–194. N.S. Dhalla, editor. University Park Press, Baltimore
Valdiosera, R., Clausen, C., Eisenberg, R.S. 1974. Impedance of frog skeletal muscle fibers in various solutions.J. Gen. Physiol. 63:460–491
Verrecke, J., Isenberg, G., Carmeliet, E. 1980. K efflux through inward rectifying K channels in voltage clamped Purkinje fibers.Pfluegers Arch. 384:207–217
Weidmann, S. 1970. Electrical constants of trabecular muscle from mammalian heart.J. Physiol. (London) 210:1041–1054
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Moore, L.E., Schmid, A. & Isenberg, G. Linear electrical properties of isolated cardiac cells. J. Membrain Biol. 81, 29–40 (1984). https://doi.org/10.1007/BF01868807
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DOI: https://doi.org/10.1007/BF01868807