Use of topological charge to determine filament location and dynamics in a numerical model of scroll wave activity

The unique time course of an excitable element in cardiac tissue can be represented as the phase of its trajectory in state space. A phase singularity is defined as a spatial point where the surrounding phase values changes by a total of 2/spl pi/, thereby forming the organizing center for a reentrant excitatory wave, a phenomenon which occurs in cardiac fibrillation. In this paper, we describe a methodology to detect the singular filament in numeric simulations of three-dimensional (3-D) scroll waves by using the concept of topological charge. Here, we use simple two-variable models of cardiac activity to construct the state space, generate the phase field, and calculate the topological charge as a summation of 3-D convolution operations. We illustrate the usage of the algorithm on the basic dynamics of vortex ring filament behavior as well as the more complex spatiotemporal behavior observed in fibrillation. We also compare the motion of filament wavetips as determined by the phase field produced by two-variable state space and single-variable, time-delay embedded state space. Finally, we examine the state spaces produced by a more complex three-variable model. We conclude that the use of state-space analysis, along with the unique properties of topological charge, allows for a novel means of filament localization.

[1]  M. Vinson,et al.  Interactions of spiral waves in inhomogeneous excitable media , 1998 .

[2]  J Jalife,et al.  Spiral waves in two-dimensional models of ventricular muscle: formation of a stationary core. , 1998, Biophysical journal.

[3]  J. Kurths,et al.  Phase Synchronization of Chaotic Oscillators by External Driving , 1997 .

[4]  Flavio H. Fenton,et al.  Fiber-Rotation-Induced Vortex Turbulence in Thick Myocardium , 1998 .

[5]  A. Pertsov,et al.  [Vortex ring in a 3-dimensional active medium described by reaction-diffusion equations]. , 1984, Doklady Akademii nauk SSSR.

[6]  A Garfinkel,et al.  Scroll wave dynamics in a three-dimensional cardiac tissue model: roles of restitution, thickness, and fiber rotation. , 2000, Biophysical journal.

[7]  R. Gray,et al.  Spatial and temporal organization during cardiac fibrillation , 1998, Nature.

[8]  F. Fenton,et al.  Vortex dynamics in three-dimensional continuous myocardium with fiber rotation: Filament instability and fibrillation. , 1998, Chaos.

[9]  P. Wolf,et al.  Stimulus-induced critical point. Mechanism for electrical initiation of reentry in normal canine myocardium. , 1989, The Journal of clinical investigation.

[10]  A. Panfilov,et al.  Nonstationary vortexlike reentrant activity as a mechanism of polymorphic ventricular tachycardia in the isolated rabbit heart. , 1995, Circulation.

[11]  O. Berenfeld,et al.  Dynamics of intramural scroll waves in three-dimensional continuous myocardium with rotational anisotropy. , 1999, Journal of theoretical biology.

[12]  Arun V. Holden,et al.  Tension of organizing filaments of scroll waves , 1994, Philosophical Transactions of the Royal Society of London. Series A: Physical and Engineering Sciences.

[13]  R. Gray,et al.  Shock-induced figure-of-eight reentry in the isolated rabbit heart. , 1999, Circulation research.

[14]  C. Luo,et al.  A dynamic model of the cardiac ventricular action potential. II. Afterdepolarizations, triggered activity, and potentiation. , 1994, Circulation research.

[15]  J. Jalife,et al.  Cardiac Electrophysiology: From Cell to Bedside , 1990 .

[16]  S. F. Mironov,et al.  Visualizing excitation waves inside cardiac muscle using transillumination. , 2001, Biophysical journal.

[17]  T. Cochrane,et al.  When Time Breaks Down : The Three-Dimensional Dynamics of Electrochemical Waves and Cardiac Arrhythmias , 1987 .

[18]  J Jalife,et al.  Distribution of excitation frequencies on the epicardial and endocardial surfaces of fibrillating ventricular wall of the sheep heart. , 2000, Circulation research.

[19]  Stefan Müller,et al.  Three dimensional reconstruction of organizing centers in excitable chemical media , 1993 .

[20]  A. T. Winfree,et al.  Quantitative optical tomography of chemical waves and their organizing centers. , 1996, Chaos.

[21]  J P Wikswo,et al.  Quatrefoil Reentry in Myocardinm: An Optical Imaging Study of the Induction Mechanism , 1999, Journal of cardiovascular electrophysiology.

[22]  P. Wolf,et al.  Mechanism of Ventricular Vulnerability to Single Premature Stimuli in Open‐Chest Dogs , 1988, Circulation research.

[23]  J Jalife,et al.  Topological constraint on scroll wave pinning. , 2000, Physical review letters.

[24]  Aaas News,et al.  Book Reviews , 1893, Buffalo Medical and Surgical Journal.

[25]  A. Winfree,et al.  Electrical turbulence in three-dimensional heart muscle. , 1994, Science.

[26]  S. Pogwizd,et al.  Mechanisms underlying the development of ventricular fibrillation during early myocardial ischemia. , 1990, Circulation research.

[27]  R. Aliev,et al.  A simple two-variable model of cardiac excitation , 1996 .

[28]  Fraser,et al.  Independent coordinates for strange attractors from mutual information. , 1986, Physical review. A, General physics.

[29]  R. A. Gray,et al.  Ventricular fibrillation and atrial fibrillation are two different beasts. , 1998, Chaos.

[30]  G. W. Beeler,et al.  Reconstruction of the action potential of ventricular myocardial fibres , 1977, The Journal of physiology.

[31]  F. Takens Detecting strange attractors in turbulence , 1981 .

[32]  Arkady M. Pertsov,et al.  Dynamics of scroll rings in a parameter gradient , 1999 .

[33]  R. Gray,et al.  An Experimentalist's Approach to Accurate Localization of Phase Singularities during Reentry , 2004, Annals of Biomedical Engineering.

[34]  R. FitzHugh Impulses and Physiological States in Theoretical Models of Nerve Membrane. , 1961, Biophysical journal.

[35]  Kapral,et al.  Spiral waves in chaotic systems. , 1996, Physical review letters.

[36]  C. Luo,et al.  A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. , 1994, Circulation research.

[37]  Richard A. Gray,et al.  SPIRAL WAVES AND THE HEART , 1996 .

[38]  B. Roth,et al.  Experimental and Theoretical Analysis of Phase Singularity Dynamics in Cardiac Tissue , 2001, Journal of cardiovascular electrophysiology.

[39]  I R Efimov,et al.  Evidence of Three‐Dimensional Scroll Waves with Ribbon‐Shaped Filament as a Mechanism of Ventricular Tachycardia in the Isolated Rabbit Heart , 1999, Journal of cardiovascular electrophysiology.

[40]  M. Shashkov,et al.  Natural discretizations for the divergence, gradient, and curl on logically rectangular grids☆ , 1997 .

[41]  Arun V. Holden,et al.  THREE-DIMENSIONAL ASPECTS OF RE-ENTRY IN EXPERIMENTAL AND NUMERICAL MODELS OF VENTRICULAR FIBRILLATION , 1999 .

[42]  A. Panfilov,et al.  Spiral breakup as a model of ventricular fibrillation. , 1998, Chaos.

[43]  R. Gray,et al.  Video imaging of atrial defibrillation in the sheep heart. , 1997, Circulation.

[44]  Ying-Cheng Lai,et al.  PHASE CHARACTERIZATION OF CHAOS , 1997 .

[45]  N. D. Mermin,et al.  The topological theory of defects in ordered media , 1979 .

[46]  A V Panfilov,et al.  Modeling of heart excitation patterns caused by a local inhomogeneity. , 1996, Journal of theoretical biology.