The role of photon scattering in voltage-calcium fluorescent recordings of ventricular fibrillation.

Recent optical mapping studies of cardiac tissue suggest that membrane voltage (V(m)) and intracellular calcium concentrations (Ca) become dissociated during ventricular fibrillation (VF), generating a proarrhythmic substrate. However, experimental methods used in these studies may accentuate measured dissociation due to differences in fluorescent emission wavelengths of optical voltage/calcium (V(opt)/Ca(opt)) signals. Here, we simulate dual voltage-calcium optical mapping experiments using a monodomain-Luo-Rudy ventricular-tissue model coupled to a photon-diffusion model. Dissociation of both electrical, V(m)/Ca, and optical, V(opt)/Ca(opt), signals is quantified by calculating mutual information (MI) for VF and rapid pacing protocols. We find that photon scattering decreases MI of V(opt)/Ca(opt) signals by 23% compared to unscattered V(m)/Ca signals during VF. Scattering effects are amplified by increasing wavelength separation between fluorescent voltage/calcium signals and respective measurement-location misalignment. In contrast, photon scattering does not affect MI during rapid pacing, but high calcium dye affinity can decrease MI by attenuating alternans in Ca(opt) but not in V(opt). We conclude that some dissociation exists between voltage and calcium at the cellular level during VF, but MI differences are amplified by current optical mapping methods.

[1]  G Plank,et al.  Computational tools for modeling electrical activity in cardiac tissue. , 2003, Journal of electrocardiology.

[2]  C. Luo,et al.  A model of the ventricular cardiac action potential. Depolarization, repolarization, and their interaction. , 1991, Circulation research.

[3]  L. Clerc Directional differences of impulse spread in trabecular muscle from mammalian heart. , 1976, The Journal of physiology.

[4]  Lei Ding,et al.  Quantifying spatial localization of optical mapping using Monte Carlo simulations , 2001, IEEE Transactions on Biomedical Engineering.

[5]  A. Welch,et al.  A review of the optical properties of biological tissues , 1990 .

[6]  Olivier Bernus,et al.  Dual excitation wavelength epifluorescence imaging of transmural electrophysiological properties in intact hearts. , 2010, Heart rhythm.

[7]  Gernot Plank,et al.  Representing Cardiac Bidomain Bath-Loading Effects by an Augmented Monodomain Approach: Application to Complex Ventricular Models , 2011, IEEE Transactions on Biomedical Engineering.

[8]  Computational modeling of cardiac dual calcium-voltage optical mapping , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[9]  Frederick J Vetter,et al.  Optical Action Potential Upstroke Morphology Reveals Near-Surface Transmural Propagation Direction , 2005, Circulation research.

[10]  A Garfinkel,et al.  Intracellular Ca(2+) dynamics and the stability of ventricular tachycardia. , 1999, Biophysical journal.

[11]  Blanca Rodriguez,et al.  Synthesis of voltage-sensitive optical signals: application to panoramic optical mapping. , 2006, Biophysical journal.

[12]  Yordan Kostov,et al.  Fluorescence imaging of electrical activity in cardiac cells using an all-solid-state system , 2004, IEEE Transactions on Biomedical Engineering.

[13]  Alan Garny,et al.  An investigation into the role of the optical detection set-up in the recording of cardiac optical mapping signals: A Monte Carlo simulation study , 2009 .

[14]  J. Wikswo,et al.  Examination of optical depth effects on fluorescence imaging of cardiac propagation. , 2003, Biophysical journal.

[15]  J. Weiss,et al.  Dissociation of Membrane Potential and Intracellular Calcium during Ventricular Fibrillation , 2005, Journal of cardiovascular electrophysiology.

[16]  J Jalife,et al.  Ventricular fibrillation: mechanisms of initiation and maintenance. , 2000, Annual review of physiology.

[17]  Boris Kogan,et al.  Intracellular Ca dynamics in ventricular fibrillation. , 2004, American journal of physiology. Heart and circulatory physiology.

[18]  Natalia A Trayanova,et al.  The role of photon scattering in optical signal distortion during arrhythmia and defibrillation. , 2007, Biophysical journal.

[19]  D. Rosenbaum,et al.  Unique Properties of Cardiac Action Potentials Recorded with Voltage‐Sensitive Dyes , 1996, Journal of cardiovascular electrophysiology.

[20]  A. Pertsov,et al.  Detection of intramyocardial scroll waves using absorptive transillumination imaging. , 2007, Journal of biomedical optics.

[21]  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.

[22]  A. G. Shvedko,et al.  Spatiotemporal Relationship Between Intracellular Ca2+ Dynamics and Wave Fragmentation During Ventricular Fibrillation in Isolated Blood-Perfused Pig Hearts , 2007, Circulation research.

[23]  Leslie M. Loew,et al.  Single-sensor system for spatially resolved, continuous, and multiparametric optical mapping of cardiac tissue , 2011, Heart rhythm.