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Authors
Tim De Coster
Antoine A.F. de Vries
Daniël A. Pijnappels
Alexander V. Panfilov
Our heart beats because electrical excitation waves travel through cardiac tissue in a highly organized way. Normally, these waves originate from the heart's natural pacemaker and propagate through the heart to coordinate its contraction. However, electrical waves do not always follow this orderly pattern. Under the right conditions, they can start circulating through the tissue and form striking spatial patterns such as spirals. These patterns are not just beautiful examples of complex dynamics. They are directly relevant to cardiac arrhythmias. A rotating excitation wave can repeatedly activate the surrounding cardiac tissue instead of allowing the normal rhythm to take over, potentially maintaining an abnormally fast heartbeat.
Imagine dropping a stone into water. Circular waves spread outward from the point where the stone hits the surface. Electrical excitation in cardiac tissue can behave somewhat similarly: activation starting at one location propagates outward through the surrounding cells. Things become more interesting when such a wave is broken. Instead of simply disappearing, the free end of the excitation wave can curl around and begin rotating (opposite from a water wave). The result is a spiral wave. Each rotation produces another wave of electrical excitation, allowing the pattern to sustain itself. Spiral waves are a general phenomenon in so-called excitable media and were originally studied in chemical systems. The heart is also an excitable medium, but here these patterns have an important biological consequence: spiral waves and their three-dimensional counterparts, scroll waves, can underlie cardiac arrhythmias.
Not every rotating excitation pattern consists of a single spiral. Cardiac tissue can produce considerably more complicated structures. One example is figure-of-eight reentry, in which two counter-rotating waves form a pattern resembling the number eight. Another is a double-armed spiral, where two excitation fronts rotate around a common centre. Even more complex patterns involving several interacting waves can occur during severe rhythm disorders such as fibrillation. These different patterns demonstrate that apparently chaotic cardiac electrical activity can contain recognizable spatial structures.
Electrical excitation propagates across cardiac tissue very quickly, making these patterns difficult to observe directly. One way of visualizing them is optical mapping. Cardiac cells are loaded with voltage-sensitive fluorescent dyes and recorded using sensitive cameras. Changes in fluorescence reveal changes in the electrical voltage of the cells. This makes it possible to reconstruct electrical activity across an entire piece of cardiac tissue and literally watch excitation waves propagate, rotate, collide and disappear. Cultures of cardiac cells provide particularly useful experimental systems for studying these phenomena because their electrical activity can be visualized across a two-dimensional surface.
Real hearts are, of course, considerably more complicated than a flat layer of cells. They have a complex three-dimensional anatomy, and electrical propagation depends on properties such as cardiac geometry and the orientation of muscle fibres. For this reason, experimental observations can be complemented by multiscale computer models of the heart. These models combine the electrical behaviour of individual cardiac cells with realistic cardiac anatomy and allow us to investigate how excitation patterns behave in three dimensions. Such simulations show that the fundamental wave phenomena observed in simplified experimental preparations can also appear in realistic heart geometries.
Cardiac arrhythmias are ultimately disorders of electrical wave propagation. Looking at them as spatial patterns therefore provides a different perspective from looking only at an electrocardiogram or at the electrical properties of individual cells. Spiral waves, figure-of-eight reentry, multi-armed spirals and related excitation patterns help us understand how an initially organized electrical system can develop into a persistent arrhythmia. Combining experiments, optical mapping and computational modelling allows these patterns to be studied from individual cardiac cells all the way up to the whole heart. Apart from their medical importance, these waves are also fascinating examples of how complex patterns can spontaneously emerge from relatively simple interactions between neighbouring cells.