Abstract
Cardiac fibrillation (spontaneous, asynchronous contractions of cardiac muscle fibres) is the leading cause of death in the industrialized world1, yet it is not clear how it occurs. It has been debated whether or not fibrillation is a random phenomenon. There is some determinism during fibrillation2,3, perhaps resulting from rotating waves of electrical activity4,5,6. Here we present a new algorithm that markedly reduces the amount of data required to depict the complex spatiotemporal patterns of fibrillation. We use a potentiometric dye7 and video imaging8,9 to record the dynamics of transmembrane potentials at many sites during fibrillation. Transmembrane signals at each site exhibit a strong periodic component centred near 8 Hz. This periodicity is seen as an attractor in two-dimensional-phase space and each site can be represented by its phase around the attractor. Spatial phase maps at each instant reveal the ‘sources’ of fibrillation in the form of topological defects, or phase singularities10, at a few sites. Using our method of identifying phase singularities, we can elucidate the mechanisms for the formation and termination of these singularities, and represent an episode of fibrillation by locating singularities. Our results indicate an unprecedented amount of temporal and spatial organization during cardiac fibrillation.
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References
Myerburg, R. J. et al. in Cardiac Electrophysiology, From Cell to Bedside (W. B. Saunders, Philadelphia, (1990)).
Garfinkel, A. et al. Quasiperiodicity and chaos in cardiac fibrillation. J. Clin. Invest. 99, 305–314 (1997).
Witkowski, F. X. et al. Evidence for determinism in ventricular fibrillation. Phys. Rev. Lett. 75, 1230–1233 (1995).
Gray, R,. A., et al. Mechanisms of cardiac fibrillation. Science 270, 1222–1223 (1995).
Ikeda, T. et al. Mechanism of spontaneous termination of functional reentry in isolated canine right atrium. Circulation 94, 1962–1973 (1996).
Lee, J. J. et al. Reentrant wavefronts in Wiggers' stage II ventricular fibrillation. Circ. Res. 78, 660–675 (1996).
Salzberg, B. M., Davila, H. V. & Cohen, L. B. Optical recordings of impulses in individual neurons of an invertebrate central nervous system. Nature 246, 508–509 (1973).
Davidenko, J. M., Pertsov, A. M., Salomonsz, R., Baxter, W. T. & Jalife, J. Stationary and drifting spiral waves of excitation in isolated cardiac muscle. Nature 355, 349–351 (1991).
Pertsov, A. M., Davidenko, J. M., Salomonsz, R., Baxter, W. T. & Jalife, J. Spiral waves of excitation underlie reentrant activity in isolated cardiac muscle. Circ. Res. 72, 631–650 (1993).
Winfree, A. T. When Time Breaks Down. (Princeton Univ. Press, (1987)).
Winfree, A. T. Scroll-shaped waves of chemical activity in three dimensions. Science 181, 937–939 (1973).
Goldbeter, A. Mechanism for oscillatory synthesis of cAMP in Dictyostelium discoideum. Nature 253, 540–542 (1975).
Lechleiter, J., Girdad, S. & Peralta, E. Spiral calcium wave propagation and annihilation in Xenopus laevis oocytes. Science 252, 123–125 (1991).
Gray, R. A. et al. Non-stationary vortex-like reentry as a mechanism of polymorphic ventricular tachycardia in the isolated rabbit heart. Circulation 91, 2454–2469 (1995).
Winfree, A. T. Electrical turbulence in three-dimensional heart muscle. Science 266, 1003–1006 (1994).
Moe, G. K. & Abildskov, J. A. Atrial fibrillation as a self-sustaining arrhythmia independent of focal discharge. Am. Heart J. 58, 59–70 (1959).
Allessie, M. A., Lammers, W., Bonke, F. I. M. & Hollen, J. in Cardiac Electrophysiology and Arrhythmias 265–275 (Grune and Stratton, Orlando, (1985)).
Krinsky, V. I. Mathematical models of cardiac arrhythmias (spiral waves). Pharmacol. Ther. B 3, 539–555 (1978).
Zykov, V. S. Simulation of Wave Processes in Excitable Media. (University Press, New York/Manchester, (1987)).
Gray, R. A. & Jalife, J. Spiral waves and the heart. Int. J. Bifurc. Chaos 6, 415–435 (1996).
Bayly, P. V. et al. Efficient electrode spacing for examining spatial organization during ventricular fibrillation. J. Cardiovasc. Electrophysiol. 4, 533–546 (1993).
Bove, R. T. & Dillon, S. M. Anew high performance system for imaging cardiac electrical activity. Circulation 94, I–714 (1996).
Cha, Y. M., Birgersdotter-Green, U., Wolf, P. L., Peters, B. B. & Chen, P. S. The mechanism of termination of reentrant activity in ventricular fibrillation. Circ. Res. 74, 495–506 (1994).
Glass, L. & Mackay, M. C. From Clocks to Chaos (Princeton Univ. Press, (1988)).
Agladze, K. I. & Krinsky, V. I. Multi-armed vortices in an active chemical medium. Nature 296, 424–426 (1982).
Fast, V. G. & Pertsov, A. M. Drift of a vortex in the myocardium. Biophysics 35, 489–494 (1990).
Gotoh, M. et al. Cellular graded responses and ventricular vulnerability to reentry by a premature stimulus in isolated canine ventricle. Circulation 95, 2141–2154 (1997).
Gray, R. A., Ayers, G. & Jalife, J. Video imaging of atrial defibrillation in the sheep heart. Circulation 95, 1038–1047 (1997).
Takens, F. in Dynamical Systems and Turbulence (eds Rand, D. A. & Young, L. S.) Lecture Notes in Mathematics 898, 366–381 (Springer, Berlin, (1981)).
Fitzhugh, R. Impulses and physiological states in theoretical models of nerve membrane. Biophys. J. 1, 445–446 (1961).
Acknowledgements
We thank O. Berenfield, Z. Silverman, J. Jiang and M. Flanagan for technical assistance and M. Vinson for reading the manuscript. This work was supported by grants from the Whitaker Foundation and the N.I.H.
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Gray, R., Pertsov, A. & Jalife, J. Spatial and temporal organization during cardiac fibrillation. Nature 392, 75–78 (1998). https://doi.org/10.1038/32164
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DOI: https://doi.org/10.1038/32164
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