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How the anisotropy of the intracellular and extracellular conductivities influences stimulation of cardiac muscle

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Abstract

The bidomain model, which describes the behavior of many electrically active tissues, is equivalent to a multi-dimensional cable model and can be represented by a network of resistors and capacitors. For a two-dimensional sheet of tissue, the intracellular and extracellular conductivity tensors can be visualized as two ellipses. For any pair of conductivity tensors, a coordinate transformation can be found that reduces the extracellular ellipse to a circle and aligns the intracellular ellipse with the coordinate axes. The eccentricity of the intracellular ellipse in this new coordinate system is an important parameter. It can have two special values: zero (in which case the tissue has equal anisotropy ratios) or one (in which case the tissue is comprised of one-dimensional fibers coupled through the two-dimensional extracellular space). Thus the bidomain model provides a unifying framework within which the electrical behavior of a wide variety of nerve and muscle tissues can be studied.

When the anisotropy ratios in the intracellular and extracellular domains are not equal, stimulation with an anode always causes depolarization of some region of tissue. An analogous effect occurs in models that describe one-dimensional fibers, in which an “activating function” determines the site of stimulation. Experiments indicate that cardiac muscle does not have equal anisotropy ratios. Therefore, models developed to describe stimulation of axons may also help in understanding stimulation of two- or three-dimensional cardiac tissue, and may explain the concept of anodal stimulation of cardiac tissue through a “virtual cathode”.

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References

  1. Altman, K. W., Plonsey, R.: Development of a model for point source electrical fibre bundle stimulation. Med. Biol. Eng. Comput. 26, 466–475 (1988)

    Google Scholar 

  2. Altman, K. W., Plonsey, R.: Point source nerve bundle stimulation: Effects of fiber diameter and depth on simulated excitation. IEEE Trans. Biomed. Eng. 37, 688–698 (1990)

    Google Scholar 

  3. Aravind, P. K.: Geometrical interpretation of the simultaneous diagonalization of two quadratic forms. Am. J. Phys. 57, 309–311 (1989)

    Google Scholar 

  4. Barr, R. C., Plonsey, R.: Propagation of excitation in idealized anisotropic two-dimensional tissue. Biophys. J. 45, 1191–1202 (1984)

    Google Scholar 

  5. Clerc, L.: Directional differences of impulse spread in trabecular muscle from mammalian heart. J. Physiol. 255, 335–346 (1976)

    Google Scholar 

  6. Colli Franzone, P., Guerri, L., Rovida, S.: Wavefront propagation in an activation model of the anisotropic cardiac tissue: Asymptotic analysis and numerical simulations. J. Math. Biol. 28, 121–176 (1990)

    Google Scholar 

  7. Colli Franzone, P., Guerri, L., Tentoni, S.: Mathematical modeling of the excitation process in myocardial tissue: Influence of fiber rotation on wavefront propagation and potential field. Math. Biosci. 101, 155–235 (1990)

    Google Scholar 

  8. Dekker, E.: Direct current make and break thresholds for pacemaker electrodes on the canine ventricle. Circ. Res. 27, 811–823 (1970)

    Google Scholar 

  9. Eisenberg, R. S., Barcilon, V., Mathias, R. T.: Electrical properties of spherical syncytia. Biophys. J. 48, 449–460 (1979)

    Google Scholar 

  10. Geselowitz, D. B., Miller, W. T., III: A bidomain model for anisotropic cardiac muscle. Ann. Biomed. Eng. 11, 191–206 (1982)

    Google Scholar 

  11. Geselowitz, D. B., Barr, R. C., Spach, M. S., Miller, W. T., III: The impact of adjacent isotropic fluids on electrograms from anisotropic cardiac muscle. A modeling study. Circ. Res. 51, 602–613 (1982)

    Google Scholar 

  12. Goldstein, H.: Classical Mechanics. Reading, Mass.: Addison-Wesley 1981

    Google Scholar 

  13. Goto, M., Brooks, C. McC.: Membrane excitability of the frog ventricle examined by long pulses. Am. J. Physiol. 217, 1236–1245 (1969)

    Google Scholar 

  14. Henriquez, C. S., Plonsey, R.: Effect of resistive discontinuities on waveshape and velocity in a single cardiac fibre. Med. Biol. Eng. Comput. 25, 428–438 (1987)

    Google Scholar 

  15. Henriquez, C. S., Plonsey, R.: Simulation of propagation along a cylindrical bundle of cardiac tissue — I: Mathematical formulation. IEEE Trans. Biomed. Eng. 37, 850–860 (1990)

    Google Scholar 

  16. Henriquez, C. S., Plonsey, R.: Simulation of propagation along a cylindrical bundle of cardiac tissue — II: Results of Simulation. IEEE Trans. Biomed. Eng. 37, 861–875 (1990)

    Google Scholar 

  17. Henriquez, C. S., Trayanova, N., Plonsey, R.: Potential and current distributions in a cylindrical bundle of cardiac tissue. Biophys. J. 53, 907–918 (1988)

    Google Scholar 

  18. Henriquez, C. S., Trayanova, N., Plonsey, R.: A planar slab model for cardiac tissue. Ann. Biomed. Eng. 18, 367–376 (1990)

    Google Scholar 

  19. Hoshi, T., Matsuda, K.: Excitability cycle of cardiac muscle examined by intracellular stimulation. Jpn. J. Physiol. 12, 433–446 (1962)

    Google Scholar 

  20. Jack, J. J. B., Noble, D., Tsien, R. W.: Electric Current Flow in Excitable Cells. Oxford, UK: Clarendon Press 1975

    Google Scholar 

  21. Keener, J. P.: On the formation of circulating patterns of excitation in anisotropic excitable media. J. Math. Biol. 26, 41–56 (1988)

    Google Scholar 

  22. Krassowska, W., Pilkington, T. C., Ideker, R. E.: The closed form solution to the periodic core-conductor model using asymptotic analysis. IEEE Trans. Biomed. Eng. 34, 519–531 (1987)

    Google Scholar 

  23. Krassowska, W., Pilkington, T. C., Ideker, R. E.: Periodic conductivity as a mechanism for cardiac stimulation and defibrillation. IEEE Trans. Biomed. Eng. 34, 555–560 (1987)

    Google Scholar 

  24. Krassowska, W., Pilkington, T. C., Ideker, R. E.: Modelling the periodicity of cardiac muscle. J. Electrocardiol. 22 (Suppl), 41–47 (1989)

    Google Scholar 

  25. Krassowska, W., Pilkington, T. C., Ideker, R. E.: Potential distribution in three-dimensional periodic myocardiuim — Part I: Solution with two-scale asymptotic analysis. IEEE Trans. Biomed. Eng. 37, 252–266 (1990)

    Google Scholar 

  26. Krassowska, W., Pilkington, T. C., Ideker, R. E.: Potential distribution in three-dimensional periodic myocardium — Part II: Application to extracellular stimulation. IEEE Trans. Biomed. Eng. 37, 267–284 (1990)

    Google Scholar 

  27. Krassowska, W., Knisley, S. B., Pilkington, T. C., Ideker, R. E.: Modeling high-frequency pacing with a discrete cardiac strand. Proc. Annu. Conf. IEEE Eng. Med. Biol. Soc. 12, 624–625 (1990)

    Google Scholar 

  28. Landau, L., Lifshitz, E.: Electrodynamics of Continuous Media. New York: Pergamon Press 1960

    Google Scholar 

  29. Leon, L. J., Horacek, B. M.: Computer model of excitation and recovery in the anisotropic myocardium. I. Rectangular and cubic arrays of excitable elements. J. Electrocardiol. 24, 1–15 (1991)

    Google Scholar 

  30. Leon, L. J., Horacek, B. M.: Computer model of excitation and recovery in the anisotropic myocardium. II. Excitation in the simplified left ventricle. J. Electrocardiol. 24, 17–31 (1991)

    Google Scholar 

  31. Leon, L. J., Horacek, B. M.: Computer model of excitation and recovery in the anisotropic myocardium. III. Arrhythmogenic conditions in the simplified left ventricle. J. Electrocardiol. 24, 33–41 (1991)

    Google Scholar 

  32. Mathias, R. T.: Steady-state voltages, ion fluxes, and volume regulation in syncytial tissues. Biophys. J. 48, 435–448 (1985)

    Google Scholar 

  33. Miller, W. T. III, Geselowtiz, D. B.: Simulation studies of the electrocardiogram, I. The normal heart. Circ. Res. 43, 301–315 (1978)

    Google Scholar 

  34. Muler, A. L., Markin, V. S.: Electrical properties of anisotropic nerve-muscle syncytia — I. Distribution of the electrotronic potential. Biofizika 22, 307–312 (1977)

    Google Scholar 

  35. Muler, A. L., Markin, V. S.: Electrical properties of anisotropic nerve-muscle syncytia — II. Spread of flat front of excitation. Biofizika 22, 518–522 (1977)

    Google Scholar 

  36. Muler, A. L., Markin, V. S.: Electrical properties of anisotropic nerve-muscle syncytia — III. Steady form of the excitation front. Biofizika 22, 671–675 (1977)

    Google Scholar 

  37. Peskoff, A.: Electric potential in three-dimensional electrically syncytial tissues. Bull. Math. Biol. 41, 163–181 (1979)

    Google Scholar 

  38. Peskoff, A.: Electric potential in cylindrical syncytia and muscle fibers. Bull. Math. Biol. 41, 183–192 (1979)

    Google Scholar 

  39. Plonsey, R.: The use of a bidomain model for the study of excitable media. Lect. Math. Life Sci. 21, 123–149 (1989)

    Google Scholar 

  40. Plonsey, R., Barr, R. C.: The four-electrode resistivity technique as applied to cardiac muscle. IEEE Trans. Biomed. Eng. 29, 541–546 (1982)

    Google Scholar 

  41. Plonsey, R., Barr, R. C.: Effect of microscopic and macroscopic discontinuities on the response of cardiac tissue to defibrillating (stimulating) currents. Med. Biol. Eng. Comput. 24, 130–136 (1986)

    Google Scholar 

  42. Plonsey, R., Barr, R. C.: Inclusion of junction elements in a linear cardiac model through secondary sources. Application to defibrillation. Med. Biol. Eng. Comput. 24, 137–144 (1986)

    Google Scholar 

  43. Plonsey, R., Barr, R. C.: Interstitial potentials and their change with depth into cardiac tissue. Biophys. J. 51, 547–555 (1987)

    Google Scholar 

  44. Plonsey, R., Barr, R. C.: Current flow patterns in two-dimensional anisotropic bisyncytia with normal and extreme conductivities. Biophys. J. 45, 557–571 (1984)

    Google Scholar 

  45. Rattay, F.: Ways to approximate current-distance relations for electrically stimulated fibers. J. Theor. Biol. 125, 339–349 (1987)

    Google Scholar 

  46. Roberts, D. E., Hersh, L. T., Scher, A. M.: Influence of cardiac fiber orientation on wavefront voltage, conduction velocity, and tissue resistivity in the dog. Circ. Res. 44, 701–712 (1979)

    Google Scholar 

  47. Roberts, D. E., Scher, A. M.: Effects of tissue anisotropy on extracellular potential fields in canine myocardium in situ. Circ. Res. 50, 342–351 (1982)

    Google Scholar 

  48. Roth, B. J.: The electrical potential produced by a strand of cardiac muscle: A bidomain analysis. Ann. Biomed. Eng. 16, 609–637 (1988)

    Google Scholar 

  49. Roth, B. J.: Action potential propagation in a thick strand of cardiac muscle. Circ. Res. 68, 162–173 (1991)

    Google Scholar 

  50. Roth, B. J., Wikswo, J. P. Jr.: A bi-domain model for the extracellular potential and the magnetic field of cardiac tissue. IEEE Trans. Biomed. Eng. 32, 467–469 (1986)

    Google Scholar 

  51. Roth, B. J., Guo, W.-Q., Wikswo, J. P. Jr.: The effects of spiral anisotropy on the electrical potential and magnetic field at the apex of the heart. Math. Biosci. 88, 159–189 (1988)

    Google Scholar 

  52. Roth, B. J., Gielen, F. L. H.: A comparison of two models for calculating the electrical potential in skeletal muscle. Ann. Biomed. Eng. 15, 591–602 (1987)

    Google Scholar 

  53. Rudy, Y., Quan, W.: A model study of the effects of the discrete cellular structure on electrical propagation in cardiac tissue. Circ. Res. 61, 815–823 (1987)

    Google Scholar 

  54. Sepulveda, N. G., Wikswo, J. P., Jr.: Electric and magnetic fields from two-dimensional anisotropic bisyncytia. Biophys. J. 51, 557–568 (1987)

    Google Scholar 

  55. Sepulveda, N. G., Roth, B. J., Wikswo, J. P., Jr.: Current injection into a two-dimensional anisotropic bidomain. Biophys. J. 55, 987–999 (1989)

    Google Scholar 

  56. Spach, M. S., Miller, W. T., III, Geselowitz, D. B., Barr, R. C., Kootsey, J. M., Johnson, E. A.: The discontinuous nature of propagation in normal canine cardiac muscle. Evidence for recurrent discontinuities of intracellular resistance that affect the membrane currents. Circ. Res. 48, 39–54 (1981)

    Google Scholar 

  57. Tung, L.: A bi-domain model for describing ischemic myocardial d-c potentials. Ph.D. dissertation. Cambridge, Massachusetts: MIT 1978

    Google Scholar 

  58. Wikswo, J. P. Jr., Wisialowski, T. A., Altemeier, W. A., Balser, J. R., Kopelman, H. A., Roden, D. M.: Virtual cathode effects during stimulation of cardiac muscle: Two-dimensional in vivo experiments. Circ. Res. 68, 513–530 (1991)

    Google Scholar 

  59. Winfree, A. T.: Ventricular reentry in three dimensions. In: Zipes, D. P., Jalife, J. (eds.) Cardiac Electrophysiology, From Cell to Bedside, pp. 224–234. Philadelphia: Saunders 1990

    Google Scholar 

  60. Woodbury, J. W., Crill, W. E.: On the problem of impulse conduction in the atrium. In: Lord Florey (ed.) Nervous Inhibition, pp. 124–135. New York: Plenum Press 1961

    Google Scholar 

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Roth, B.J. How the anisotropy of the intracellular and extracellular conductivities influences stimulation of cardiac muscle. J. Math. Biol. 30, 633–646 (1992). https://doi.org/10.1007/BF00175610

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