Wave propagation in ventricular muscle is rendered highly anisotropic by the intramural rotation of the fiber. This rotational anisotropy is especially important because it can produce a twist of electrical vortices, which measures the rate of rotation (in degree/mm) of activation wavefronts in successive planes perpendicular to a line of phase singularity, or filament. This twist can then significantly alter the dynamics of the filament. This paper explores this dynamics via numerical simulation. After a review of the literature, we present modeling tools that include: (i) a simplified ionic model with three membrane currents that approximates well the restitution properties and spiral wave behavior of more complex ionic models of cardiac action potential (Beeler-Reuter and others), and (ii) a semi-implicit algorithm for the fast solution of monodomain cable equations with rotational anisotropy. We then discuss selected results of a simulation study of vortex dynamics in a parallelepipedal slab of ventricular muscle of varying wall thickness (S) and fiber rotation rate z). The main finding is that rotational anisotropy generates a sufficiently large twist to destabilize a single transmural filament and cause a transition to a wave turbulent state characterized by a high density of chaotically moving filaments. This instability is manifested by the propagation of localized disturbances along the filament and has no previously known analog in isotropic excitable media. These disturbances correspond to highly twisted and distorted regions of filament, or “twistons,” that create vortex rings when colliding with the natural boundaries of the ventricle. Moreover, when sufficiently twisted, these rings expand and create additional filaments by further colliding with boundaries. This instability mechanism is distinct from the commonly invoked patchy failure or wave breakup that is not observed here during the initial instability. For modified Beeler-Reuter-like kinetics with stable reentry in two dimensions, decay into turbulence occurs in the left ventricle in about one second above a critical wall thickness in the range of 4–6 mm that matches experiment. However this decay is suppressed by uniformly decreasing excitability. Specific experiments to test these results, and a method to characterize the filament density during fibrillation are discussed. Results are contrasted with other mechanisms of fibrillation and future prospects are summarized.

1.
A. T. Winfree, When Time Breaks Down (Princeton University Press, Princeton, NJ, 1987).
2.
V. Zykov, Simulation of Wave Processes in Excitable Media (Nuaka, Moscow, 1984).
3.
R.
Gray
and
J.
Jalife
, “
Spiral waves and the heart
,”
Int. J. Bifurcation Chaos Appl. Sci. Eng.
6
,
415
(
1996
).
4.
V.
Krinsky
and
A.
Pumir
, “
Models of defibrillation in cardiac tissue
,”
Chaos
8
,
188
203
(
1998
).
5.
V.
Biktashev
and
A.
Holden
, “
Re-entrant waves and their elimination in a model of mammalian ventricular tissue
,”
Chaos
8
,
48
56
(
1998
).
6.
F.
Witkowski
et al., “
A method for visualization of ventricular fibrillation: Design of a cooled fiberoptically coupled image intensified CCD data acquisition system incorporating wavelet shrinkage based adaptive filtering
,”
Chaos
8
,
94
102
(
1998
).
7.
J.
Davidenko
et al., “
Stationary and drifting spiral waves of excitation in isolated cardiac muscle
,”
Nature (London)
355
,
349
(
1992
).
8.
R.
Gray
et al., “
Nonstationary vortexlike reentrant activity as a mechanism of polymorphic ventriculoar tachycardia in the isolated rabbit heart
,”
Circulation
91
,
2454
(
1995
).
9.
P. Bayly et al., “A quantitative measurement of spatial order in ventricular fibrillation,” J. Cardiovasc. Electrophysiol. 4, 533 (1993).
10.
A.
Garfinkel
et al., “
Quasiperiodicity and chaos in cardiac fibrillation
,”
J. Clin. Invest.
99
,
1
(
1997
).
11.
D.
Noble
, “
A modification of the Hodgkin-Huxley equations applicable to Purkinje fibre action and pace-maker potentials
,”
J. Physiol. (London)
160
,
317
(
1962
).
12.
G.
Beeler
and
H.
Reuter
, “
Reconstruction of the action potential of ventricular myocardial fibres
,”
J. Physiol. (London)
268
,
177
(
1977
).
13.
D. D.
Francesco
and
D.
Noble
, “
A model of cardiac electrical activity incorporating ionic pumps and concentration changes
,”
Philos. Trans. R. Soc. London, Ser. B
307
,
353
(
1985
).
14.
C.
Luo
and
Y.
Rudy
, “
A model of the ventricular cardiac action potential
,”
Circ. Res.
68
,
1501
(
1991
).
15.
C.
Luo
and
Y.
Rudy
, “
A dynamic model of the cardiac ventricular action potential I. Simulations of ionic currents and concentration changes
,”
Circ. Res.
74
,
1071
(
1994
).
16.
C.
Henriquez
and
A.
Papazoglou
, “
Using computer models to understand the roles of tissue structure and membrane dynamics in arrhythmogenesis
,”
Proc. IEEE
84
,
334
(
1996
).
17.
M.
Boyett
and
B.
Jewell
, “
A study of the factors responsible for rate-dependent shortening of the action potential in mammalian ventricular muscle
,”
J. Physiol. (London)
285
,
359
(
1978
).
18.
V.
Elharrar
and
B.
Surawicz
, “
Cycle length effect on restitution of action potential duration in dog cardiac fibers
,”
Am. J. Physiol.
244
,
H782
(
1983
).
19.
S.
Girouard
et al., “
Optical mapping in a new guinea pig model of ventricular tachycardia reveals mechanisms for multiple wavelengths in a single reentrant circuit
,”
Circulation
93
,
603
(
1996
).
20.
C.
Thomas
, “
The muscular architecture of the ventricles of hog and dog hearts
,”
Am. J. Anat.
101
,
17
(
1957
).
21.
D. Streeter, “Gross morphology and fiber geometry in the heart,” in Handbook of Physiology, edited by R. Berne (American Physiological Society, Bethesda, MD, 1979), Vol. 1, Section 2, pp. 61–112.
22.
P.
Nielsen
,
I. L.
Grice
, and
B.
Smaill
, “
Mathematical model of geometry and fibrous structure of the heart
,”
Am. J. Physiol.
260
,
H1365
(
1991
).
23.
C.
Peskin
, “
Fiber architecture of the left ventricular wall: An asymptotic analysis
,”
Commun. Pure Appl. Math.
42
,
79
(
1989
).
24.
J.
Keener
, “
An eikonal-curvature equation for action potential propagation in myocardium
,”
J. Math. Biol.
29
,
629
(
1991
).
25.
P. Franzone, L. Guerri, and B. Taccardi, “Spread of excitation in a myocardial volume,” J. Cardiovasc. Electrophysiol. 4, 144 (1993).
26.
B.
Taccardi
,
E.
Macchi
, and
Y.
Vyhmeister
, “
Effect of myocardial fiber direction on epicardial potentials
,”
Circulation
90
,
3076
(
1994
).
27.
A.
Pollard
,
M.
Burgess
, and
K.
Spitzer
, “
Computer simulations of three-dimensional propagation in ventricular myocardium. Effects of intramural fiber rotation and inhomogeneous conductivity on epicardial activation
,”
Circ. Res.
72
,
744
(
1993
).
28.
A.
Panfilov
and
J.
Keener
, “
Re-entry in three-dimensional FitzHugh-Nagumo medium with rotational anisotropy
,”
Physica D
84
,
545
(
1995
).
29.
D. Zipes, Circulation, “Electrophysiological mechanisms involved in ventricular fibrillation,” Suppl. III 51, 120 (1975).
30.
D.
Zipes
et al., “
Termination of ventricular fibrillation in dogs by depolarizing a critical amount of myocardium
,”
Am. J. Cardiol.
36
,
37
(
1975
).
31.
K.
Kavanagh
et al., “
High-current stimuli to the spared epicardium of a large infract induce ventricular tachycardia
,”
Circulation
85
,
680
(
1992
).
32.
A. Winfree, “Rotors, fibrillation, and dimensionality,” in Computational Biology of the Heart, edited by A. Panfilov and A. Holden (Wiley, New York, 1997), pp. 101–135.
33.
A.
Winfree
, “
Electrical turbulence in three-dimensional heart muscle
,”
Science
266
,
1003
(
1994
).
34.
A.
Winfree
, “
Stable particle-like solutions to the nonlinear wave equations of three-dimensional excitable media
,”
SIAM (Soc. Ind. Appl. Math.) Rev.
32
,
1
(
1990
).
35.
A.
Mikhailov
,
A.
Panfilov
, and
A.
Rudenko
, “
Twisted scroll waves in active three-dimensional media
,”
Phys. Lett. A
109
,
246
(
1985
).
36.
J.
Keener
, “
The dynamics of three-dimensional scroll waves in excitable media
,”
Physica D
31
,
269
(
1988
).
37.
V.
Biktashev
, “
Evolution of twist of an autowave vortex
,”
Physica D
36
,
167
(
1989
).
38.
J.
Keener
and
J.
Tyson
, “
The dynamics of scroll waves in excitable media
,”
SIAM (Soc. Ind. Appl. Math.) Rev.
34
,
1
(
1992
).
39.
V.
Biktashev
,
A.
Holden
, and
H.
Zhang
, “
Tension of organizing filaments of scroll waves
,”
Philos. Trans. R. Soc. London, Ser. A
347
,
611
(
1994
).
40.
C.
Henze
,
E.
Lugosi
, and
A.
Winfree
, “
Helical organizing centers in excitable media
,”
Can. J. Phys.
68
,
683
(
1989
).
41.
A.
Pertsov
,
R.
Aliev
, and
V.
Krinsky
, “
Three-dimensional twisted vortices in an excitable chemical medium
,”
Nature (London)
345
,
419
(
1990
).
42.
S.
Mironov
,
M.
Vinson
,
S.
Mulvey
, and
A.
Pertsov
, “
Destabilization of three-dimensional rotating chemical waves in an inhomogeneous BZ reaction
,”
J. Physiol. (London)
100
,
1975
(
1996
).
43.
A. Winfree, “Estimating the ventricular fibrillation threshold,” in Theory of Heart, edited by L. Glass, P. Hunter, and A. McCulloch (Springer-Verlag, New York, 1991), pp. 477–531.
44.
A.
Winfree
, “
Evolving perspectives during 12 years of electric turbulence
,”
Chaos
8
,
1
19
(
1998
).
45.
R.
Gray
et al., “
Mechanisms of cardiac fibrillation
,”
Science
270
,
1222
(
1995
).
46.
J.
Jalife
,
R.
Gray
,
G.
Morley
, and
J.
Davidenko
, “
Self-organization and the dynamical nature of ventricular fibrillation
,”
Chaos
8
,
79
93
(
1998
).
47.
P.
Bayly
et al., “
Spatial organization, predictability, and determinism in ventricular fibrillation
,”
Chaos
8
,
103
115
(
1998
).
48.
A.
Panfilov
and
A.
Holden
, “
Spatiotemporal irregularity in a two-dimensional model of cardiac tissue
,”
Int. J. Bifurcation Chaos Appl. Sci. Eng.
1
,
219
(
1991
).
49.
M.
Courtemanche
and
A.
Winfree
, “
Re-entrant rotating waves in a Beeler-Reuter based model of two-dimensional cardiac electrical activity
,”
Int. J. Bifurcation Chaos Appl. Sci. Eng.
1
,
431
(
1991
).
50.
M.
Courtemanche
, “
Complex spiral wave dynamics in a spatially distributed ionic model of cardiac electrical activity
,”
Chaos
6
,
579
(
1996
).
51.
J.
Leon
,
F.
Roberge
, and
A.
Vinet
, “
Simulation of two-dimensional anisotropic cardiac reentry: Effects of the wavelength on the reentry characteristics
,”
Ann. Biomed. Eng.
22
,
592
(
1994
).
52.
A.
Panfilov
and
P.
Hogeweg
, “
Spiral breakup in a modified FitzHugh-Nagumo model
,”
Phys. Lett.
176
,
295
(
1993
).
53.
A.
Karma
, “
Spiral breakup in model equations of action potential propagation in cardiac tissue
,”
Phys. Rev. Lett.
71
,
1103
(
1993
).
54.
A.
Karma
, “
Electrical alternans and spiral wave breakup in cardiac tissue
,”
Chaos
4
,
461
(
1994
).
55.
M.
Janse
, “
Vulnerability to ventricular fibrillation
,”
Chaos
8
,
149
156
(
1998
).
56.
W. Press, W. Vetterling, S. Teukolsky, and B. Flannery, Numerical Recipes Second Edition (Cambridge University Press, Cambridge, MA, 1992).
57.
R.
FitzHugh
, “
Impulses and physiological states in theoretical models of nerve membrane
,”
Biophys. J.
1
,
445
(
1961
).
58.
A.
Winfree
, “
Varieties of spiral wave behavior: An experimentalist’s approach to the theory of excitable media
,”
Chaos
1
,
303
(
1991
).
59.
A.
Panfilov
and
A.
Pertsov
,
Dokl. Akad. Nauk SSSR
274
,
1500
(
1984
).
60.
B.
Kogan
et al., “
The simplified FitzHugh-Nagumo model with action potential duration restitution
,”
Physica D
50
,
327
(
1991
).
61.
B. Kogan, W. Karplus, and M. Karpoukhin, “A third-order action potential model for computer simulation of electrical wave propagation in cardiac tissue,” in Computer Simulation in Biomedicine, edited by H. Power and R. Hart (Computational Mechanics, Boston, 1995), pp. 147–154.
62.
J.
Nolasco
and
R.
Dahlen
, “
A graphic method for the study of alternation in cardiac action potentials
,”
J. Appl. Physiol.
25
,
191
(
1968
).
63.
M. R. Guevara, G. Ward, A. Shrier, and L. Glass, “Electrical alternans and period doubling bifurcations,” in Computers in Cardiology (IEEE, 1984), pp. 167–170.
64.
H.
Ito
and
L.
Glass
, “
Theory of reentrant excitation in a ring of cardiac tissue
,”
Physica D
56
,
84
(
1992
).
65.
L.
Frame
and
M.
Simson
, “
Oscillations of conduction, action potential duration, and refractoriness
,”
Circulation
78
,
1277
(
1988
).
66.
T.
Lewis
and
M. R.
Guevara
, “
Chaotic dynamics in an ionic model of the propagated cardiac action potential
,”
J. Theor. Biol.
146
,
407
(
1990
).
67.
W.
Quan
and
Y.
Rudy
, “
Unidirectional block and reentry of cardiac excitation: A model study
,”
Circ. Res.
66
,
367
(
1990
).
68.
M.
Courtemanche
,
L.
Glass
, and
J.
Keener
, “
Instabilities of a propagating pulse in a ring of excitable media
,”
Phys. Rev. Lett.
70
,
2182
(
1993
).
69.
A.
Karma
,
H.
Levine
, and
X.
Zou
, “
Theory of pulse instabilities in electrophysiological models of excitable tissues
,”
Physica D
73
,
113
(
1994
).
70.
J.
Tyson
and
J.
Keener
, “
Singular perturbation theory of traveling waves in excitable medium
,”
Physica D
32
,
327
(
1988
).
71.
R. G.
Jr
,
N.
Otani
, and
M.
Watanabe
, “
Memory and complex dynamics in cardiac Purkinje fibers
,”
Am. J. Physiol.
272
,
H1826
(
1997
).
72.
A. Karma and F. Fenton, “Simplified ionic models of cardiac action potential” (to be published).
73.
V.
Krinsky
,
I.
Efimov
, and
J.
Jalife
, “
Vortices with linear cores in excitable media
,”
Proc. R. Soc. London, Ser. A
437
,
645
(
1992
).
74.
V.
Krinsky
and
I.
Efimov
, “
Vortices with linear cores in mathematical models of excitable media
,”
Physica A
188
,
55
(
1992
).
75.
I.
Efimov
,
V.
Krinsky
, and
J.
Jalife
, “
Dynamics of rotating vortices in the Beeler-Reuter model of cardiac tissue
,”
Chaos Solitons Fractals
5
,
513
(
1995
).
76.
F. Fenton, Ph.D. thesis, Northeastern University, Boston, MA 02115 (1998).
77.
V.
Hakim
and
A.
Karma
, “
Spiral wave meander in excitable media: The large core limit
,”
Phys. Rev. Lett.
79
,
665
(
1997
).
78.
D.
Barkley
, “
Euclidean symmetry and the dynamics of rotating spiral waves
,”
Phys. Rev. Lett.
72
,
164
(
1994
).
79.
V.
Biktashev
,
A.
Holden
, and
E.
Nikolaev
, “
Spiral wave meander and symmetry of the plane
,”
Int. J. Bifurcation Chaos Appl. Sci. Eng.
6
,
2433
(
1996
).
80.
W.
Jahnke
,
W.
Skaggs
, and
A.
Winfree
, “
Chemical vortex dynamics in the Belousov-Zhabotinsky reaction and in the two-variable oregonator model
,”
J. Phys. Chem.
93
,
740
(
1989
).
81.
V. P. G.
Li
,
Q.
Ouyang
, and
H.
Swinney
, “
Transition from simple rotating chemical spirals to meander and traveling spirals
,”
Phys. Rev. Lett.
77
,
2105
(
1996
).
82.
D.
Kim
et al., “
Electrical turbulence as a result of the critical curvature for propagation in cardiac tissue
,”
Chaos
8
,
137
148
(
1998
).
83.
S.
Dillon
,
P.
Ursell
, and
A.
Wit
, “
Pseudo-block caused by anisotropic conduction: A new mechanism for sustained reentry
,”
Circulation
72
,
1116
(
1985
).
84.
F. Fenton and A. Karma, “Rotational-anisotrophy-induced wave turbulence in thick myocardium” (to be published).
85.
H.
Hasimoto
, “
A soliton on a vortex filament
,”
J. Fluid Mech.
51
,
477
(
1972
).
86.
E.
Hopfinger
,
F.
Browand
, and
Y.
Gagne
, “
Turbulence and waves in a rotating tank
,”
J. Fluid Mech.
125
,
505
(
1982
).
87.
C.
Cabo
,
A.
Pertsov
,
J.
Davidenko
, and
J.
Jalife
, “
Electrical turbulence asa result of the critical curvature for propagation in cardiac tissue
,”
Chaos
8
,
116
126
(
1998
).
88.
J.
Keener
, “
Propagation and its failure in coupled systems of discrete excitable cells
,”
SIAM (Soc. Ind. Appl. Math.) J. Appl. Math.
47
,
556
(
1987
).
89.
J.
Keener
, “
The effects of discrete gap junction coupling on propagation in myocardium
,”
J. Theor. Biol.
148
,
19
(
1991
).
90.
A.
Panfilov
and
P.
Hogeweg
, “
Scroll breakup in a three-dimensional excitable medium
,”
Phys. Rev. E
53
,
1740
(
1996
).
91.
D.
Frazier
et al., “
Stimulus-induced critical point: Mechanism for the electrical initiation of reentry in normal canine myocardium
,”
J. Clin. Invest.
83
,
1039
(
1989
).
92.
G.
Moe
,
W.
Rheinboldt
, and
J.
Abildskov
, “
A computer model of atrial fibrillation
,”
Am. Heart J.
67
,
200
(
1964
).
93.
B. Saxberg and R. Cohen, “Cellular automata models of cardiac conduction,” in Theory of Heart, edited by L. Glass, P. Hunter, and A. McCulloch (Springer-Verlag, New York, 1991), pp. 437–476.
94.
B.
Kenneth
,
R.
Laurita
,
S.
Girouard
, and
D.
Rosenbaum
, “
Modulation of ventricular repolarization by a premature stimulus. Role of epicardial dispersion of repolarization kinetics demonstrated by optical mapping of the intact guinea pig heart
,”
Circ. Res.
79
,
493
(
1996
).
95.
M.
Vinson
,
A.
Pertsov
, and
J.
Jalife
, “
Anchoring of vortex filaments in 3d excitable media
,”
Physica D
72
,
119
(
1993
).
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