Multiarm spirals in a two-dimensional cardiac substrate

Abstract

A variety of chemical and biological nonlinear excitable media, including heart tissue, can support stable, self-organized waves of activity in a form of rotating single-arm spirals. In particular, heart tissue can support stationary and meandering spirals of electrical excitation, which have been shown to underlie different forms of cardiac arrhythmias. In contrast to single-arm spirals, stable multiarm spirals (multiple spiral waves that rotate in the same direction around a common organizing center) have not been demonstrated and studied yet in living excitable tissues. Here, we show that persistent multiarm spirals of electrical activity can be induced in monolayer cultures of neonatal rat heart cells by a short, rapid train of electrical point stimuli applied during single-arm-spiral activity. Stable formation is accomplished only in monolayers that show a relatively broad and steep dependence of impulse wavelength and propagation velocity on rate of excitation. The resulting multiarm spirals emit waves of electrical activity at rates faster than for single-arm spirals and exhibit two distinct behaviors, namely ''arm-switching'' and ''tip-switching.'' The phenomenon of rate acceleration due to an increase in the number of spiral arms possibly may underlie the acceleration of functional reentrant tachycardias paced by a clinician or an antitachycardia device.R otating single-arm spirals can exist in different chemical(1-4) and biological systems (5-8). If a spiral is stationary or weakly meandering, it represents a persistent source of highly periodic activity with a period of rotation that is determined by the properties of excitation, recovery, and diffusion in the medium. In the heart, stable single-arm spirals can underlie periodic activity such as monomorphic tachycardia, whereas unstable spirals that continuously form and break up are shown to underlie aperiodic and lethal heart activity, namely fibrillation (9). So far, stable rotating structures with a higher degree of organization, such as multiarmed spirals, have been demonstrated experimentally in chemically (2) or light-controlled (10) Belousov-Zhabotinsky reactions, in starving social amoebae Dictyostelium discoideum (11), and in FitzHugh-Nagumo-type computer models of homogenous weakly excitable media (12)(13)(14). The modes of induction of these multiarmed spirals [i.e., use of an unexcitable central obstacle that is subsequently removed (2, 10) and spontaneous formation from dense multiple wavebreaks (12) or from preset spatial distributions of excited and recovered medium (13, 14)] are not applicable to cardiac tissue. Moreover, healthy cardiac tissue exhibits normal excitability, in contrast to two-variable FitzHugh-Nagumo models, which require weak excitability to support stable multiarm spirals (12-15). In a normally excitable medium, the existence of a stable multiarm spiral as an entity distinct from negligibly interacting adjacent single spirals was questioned by Winfree (16,17), who considered that in this case distinct rates of rotat...

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