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Optical measurements reveal nature of intercellular coupling across ventricular wall

¹Heart and Vascular Research Center and Department of Biomedical Engineering, MetroHealth Campus, Case Western Reserve University, Cleveland, Ohio; and ²Department of Physics, Oakland University, Rochester, Michigan

Submitted 8 December 2004 ; accepted in final form 27 April 2005

Previously, we showed that intercellular uncoupling through gap junctions is an important mechanism for maintaining transmural heterogeneities of repolarization that are responsible for ventricular arrhythmias in disease states such as heart failure. However, rotational anisotropy between transmural muscle layers also may influence coupling. To determine the effect of rotational anisotropy on transmural coupling, we developed a numerical three-dimensional model of passive cardiac tissue in which rotational anisotropy was varied in a controlled fashion. Simulations of optical mapping demonstrated that spatial averaging produced a voltage decay in space best fit by a single decaying exponential compared with the theoretically predicted decay. As fiber orientation varied by 90° with respect to the transmural surface, the effective transmural space constant (_TM) changed by only 0.31% in simulations. In contrast, reducing intercellular conductivity by 24% decreased _TM by 7.7%. In the canine wedge preparation (n = 5), measured by optical mapping of the epicardial and subepicardial surface was similar transverse (_TV = 0.73 ± 0.10 mm) and transmural (_TM = 0.70 ± 0.08 mm) to subepicardial fibers. We confirmed previous findings that _TM in subepicardial layers was significantly reduced by 14 ± 2% compared with deeper layers of myocardium, providing evidence for transmural uncoupling in the epicardial-midmyocardial interface. These data establish the theoretical and experimental basis for measuring intercellular coupling between muscle layers spanning the ventricular wall with optical mapping techniques. Furthermore, this study demonstrates that transmural uncoupling at the epicardial-midmyocardial interface may be attributable to heterogeneous expression of cardiac gap junctions and not rotational anisotropy.

gap junction; repolarization; voltage-sensitive dyes; space constant; optical mapping; modeling

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