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. 1999 Sep;77(3):1404–1417. doi: 10.1016/S0006-3495(99)76989-4

Roles of electric field and fiber structure in cardiac electric stimulation.

S B Knisley 1, N Trayanova 1, F Aguel 1
PMCID: PMC1300429  PMID: 10465752

Abstract

This study investigated roles of the variation of extracellular voltage gradient (VG) over space and cardiac fibers in production of transmembrane voltage changes (DeltaV(m)) during shocks. Eleven isolated rabbit hearts were arterially perfused with solution containing V(m)-sensitive fluorescent dye (di-4-ANEPPS). The epicardium received shocks from symmetrical or asymmetrical electrodes to produce nominally uniform or nonuniform VGs. Extracellular electric field and DeltaV(m) produced by shocks in the absolute refractory period were measured with electrodes and a laser scanner and were simulated with a bidomain computer model that incorporated the anterior left ventricular epicardial fiber field. Measurements and simulations showed that fibers distorted extracellular voltages and influenced the DeltaV(m). For both uniform and nonuniform shocks, DeltaV(m) depended primarily on second spatial derivatives of extracellular voltages, whereas the VGs played a smaller role. Thus, 1) fiber structure influences the extracellular electric field and the distribution of DeltaV(m); 2) the DeltaV(m) depend on second spatial derivatives of extracellular voltage.

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Selected References

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  1. Baynham T. C., Knisley S. B. Effective epicardial resistance of rabbit ventricles. Ann Biomed Eng. 1999 Jan-Feb;27(1):96–102. doi: 10.1114/1.210. [DOI] [PubMed] [Google Scholar]
  2. Beeler G. W., Reuter H. Reconstruction of the action potential of ventricular myocardial fibres. J Physiol. 1977 Jun;268(1):177–210. doi: 10.1113/jphysiol.1977.sp011853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clerc L. Directional differences of impulse spread in trabecular muscle from mammalian heart. J Physiol. 1976 Feb;255(2):335–346. doi: 10.1113/jphysiol.1976.sp011283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Drouhard J. P., Roberge F. A. A simulation study of the ventricular myocardial action potential. IEEE Trans Biomed Eng. 1982 Jul;29(7):494–502. doi: 10.1109/TBME.1982.324921. [DOI] [PubMed] [Google Scholar]
  5. Efimov I. R., Cheng Y. N., Biermann M., Van Wagoner D. R., Mazgalev T. N., Tchou P. J. Transmembrane voltage changes produced by real and virtual electrodes during monophasic defibrillation shock delivered by an implantable electrode. J Cardiovasc Electrophysiol. 1997 Sep;8(9):1031–1045. doi: 10.1111/j.1540-8167.1997.tb00627.x. [DOI] [PubMed] [Google Scholar]
  6. Entcheva E., Eason J., Efimov I. R., Cheng Y., Malkin R., Claydon F. Virtual electrode effects in transvenous defibrillation-modulation by structure and interface: evidence from bidomain simulations and optical mapping. J Cardiovasc Electrophysiol. 1998 Sep;9(9):949–961. doi: 10.1111/j.1540-8167.1998.tb00135.x. [DOI] [PubMed] [Google Scholar]
  7. Entcheva E., Trayanova N. A., Claydon F. J. Patterns of and mechanisms for shock-induced polarization in the heart: a bidomain analysis. IEEE Trans Biomed Eng. 1999 Mar;46(3):260–270. doi: 10.1109/10.748979. [DOI] [PubMed] [Google Scholar]
  8. Fast V. G., Rohr S., Gillis A. M., Kléber A. G. Activation of cardiac tissue by extracellular electrical shocks: formation of 'secondary sources' at intercellular clefts in monolayers of cultured myocytes. Circ Res. 1998 Feb 23;82(3):375–385. doi: 10.1161/01.res.82.3.375. [DOI] [PubMed] [Google Scholar]
  9. Fishler M. G. Syncytial heterogeneity as a mechanism underlying cardiac far-field stimulation during defibrillation-level shocks. J Cardiovasc Electrophysiol. 1998 Apr;9(4):384–394. doi: 10.1111/j.1540-8167.1998.tb00926.x. [DOI] [PubMed] [Google Scholar]
  10. Frazier D. W., Krassowska W., Chen P. S., Wolf P. D., Dixon E. G., Smith W. M., Ideker R. E. Extracellular field required for excitation in three-dimensional anisotropic canine myocardium. Circ Res. 1988 Jul;63(1):147–164. doi: 10.1161/01.res.63.1.147. [DOI] [PubMed] [Google Scholar]
  11. Frazier D. W., Wolf P. D., Wharton J. M., Tang A. S., Smith W. M., Ideker R. E. Stimulus-induced critical point. Mechanism for electrical initiation of reentry in normal canine myocardium. J Clin Invest. 1989 Mar;83(3):1039–1052. doi: 10.1172/JCI113945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gillis A. M., Fast V. G., Rohr S., Kléber A. G. Spatial changes in transmembrane potential during extracellular electrical shocks in cultured monolayers of neonatal rat ventricular myocytes. Circ Res. 1996 Oct;79(4):676–690. doi: 10.1161/01.res.79.4.676. [DOI] [PubMed] [Google Scholar]
  13. Henriquez C. S. Simulating the electrical behavior of cardiac tissue using the bidomain model. Crit Rev Biomed Eng. 1993;21(1):1–77. [PubMed] [Google Scholar]
  14. Hill B. C., Courtney K. R. Design of a multi-point laser scanned optical monitor of cardiac action potential propagation: application to microreentry in guinea pig atrium. Ann Biomed Eng. 1987;15(6):567–577. doi: 10.1007/BF02364249. [DOI] [PubMed] [Google Scholar]
  15. Holley L. K., Knisley S. B. Transmembrane potentials during high voltage shocks in ischemic cardiac tissue. Pacing Clin Electrophysiol. 1997 Jan;20(1 Pt 2):146–152. doi: 10.1111/j.1540-8159.1997.tb04832.x. [DOI] [PubMed] [Google Scholar]
  16. Klee M., Plonsey R. Stimulation of spheroidal cells--the role of cell shape. IEEE Trans Biomed Eng. 1976 Jul;23(4):347–354. doi: 10.1109/tbme.1976.324597. [DOI] [PubMed] [Google Scholar]
  17. Knisley S. B., Baynham T. C. Line stimulation parallel to myofibers enhances regional uniformity of transmembrane voltage changes in rabbit hearts. Circ Res. 1997 Aug;81(2):229–241. doi: 10.1161/01.res.81.2.229. [DOI] [PubMed] [Google Scholar]
  18. Knisley S. B., Blitchington T. F., Hill B. C., Grant A. O., Smith W. M., Pilkington T. C., Ideker R. E. Optical measurements of transmembrane potential changes during electric field stimulation of ventricular cells. Circ Res. 1993 Feb;72(2):255–270. doi: 10.1161/01.res.72.2.255. [DOI] [PubMed] [Google Scholar]
  19. Knisley S. B., Grant A. O. Asymmetrical electrically induced injury of rabbit ventricular myocytes. J Mol Cell Cardiol. 1995 May;27(5):1111–1122. doi: 10.1016/0022-2828(95)90047-0. [DOI] [PubMed] [Google Scholar]
  20. Knisley S. B., Hill B. C. Effects of bipolar point and line stimulation in anisotropic rabbit epicardium: assessment of the critical radius of curvature for longitudinal block. IEEE Trans Biomed Eng. 1995 Oct;42(10):957–966. doi: 10.1109/10.464369. [DOI] [PubMed] [Google Scholar]
  21. Knisley S. B., Hill B. C., Ideker R. E. Virtual electrode effects in myocardial fibers. Biophys J. 1994 Mar;66(3 Pt 1):719–728. doi: 10.1016/s0006-3495(94)80846-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Knisley S. B., Smith W. M., Ideker R. E. Effect of field stimulation on cellular repolarization in rabbit myocardium. Implications for reentry induction. Circ Res. 1992 Apr;70(4):707–715. doi: 10.1161/01.res.70.4.707. [DOI] [PubMed] [Google Scholar]
  23. Knisley S. B. Transmembrane voltage changes during unipolar stimulation of rabbit ventricle. Circ Res. 1995 Dec;77(6):1229–1239. doi: 10.1161/01.res.77.6.1229. [DOI] [PubMed] [Google Scholar]
  24. Krassowska W., Pilkington T. C., Ideker R. E. Periodic conductivity as a mechanism for cardiac stimulation and defibrillation. IEEE Trans Biomed Eng. 1987 Jul;34(7):555–560. doi: 10.1109/tbme.1987.325986. [DOI] [PubMed] [Google Scholar]
  25. LeGrice I. J., Smaill B. H., Chai L. Z., Edgar S. G., Gavin J. B., Hunter P. J. Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog. Am J Physiol. 1995 Aug;269(2 Pt 2):H571–H582. doi: 10.1152/ajpheart.1995.269.2.H571. [DOI] [PubMed] [Google Scholar]
  26. Lepeschkin E., Jones J. L., Rush S., Jones R. E. Local potential gradients as a unifying measure for thresholds of stimulation, standstill, tachyarrhythmia and fibrillation appearing after strong capacitor discharges. Adv Cardiol. 1978;21:268–278. doi: 10.1159/000400463. [DOI] [PubMed] [Google Scholar]
  27. Li T., Sperelakis N., Teneick R. E., Solaro R. J. Effects of diacetyl monoxime on cardiac excitation-contraction coupling. J Pharmacol Exp Ther. 1985 Mar;232(3):688–695. [PubMed] [Google Scholar]
  28. Muzikant A. L., Henriquez C. S. Bipolar stimulation of a three-dimensional bidomain incorporating rotational anisotropy. IEEE Trans Biomed Eng. 1998 Apr;45(4):449–462. doi: 10.1109/10.664201. [DOI] [PubMed] [Google Scholar]
  29. Neunlist M., Tung L. Optical recordings of ventricular excitability of frog heart by an extracellular stimulating point electrode. Pacing Clin Electrophysiol. 1994 Oct;17(10):1641–1654. doi: 10.1111/j.1540-8159.1994.tb02359.x. [DOI] [PubMed] [Google Scholar]
  30. Neunlist M., Tung L. Spatial distribution of cardiac transmembrane potentials around an extracellular electrode: dependence on fiber orientation. Biophys J. 1995 Jun;68(6):2310–2322. doi: 10.1016/S0006-3495(95)80413-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nielsen P. M., Le Grice I. J., Smaill B. H., Hunter P. J. Mathematical model of geometry and fibrous structure of the heart. Am J Physiol. 1991 Apr;260(4 Pt 2):H1365–H1378. doi: 10.1152/ajpheart.1991.260.4.H1365. [DOI] [PubMed] [Google Scholar]
  32. Plonsey R., Barr R. C. Effect of microscopic and macroscopic discontinuities on the response of cardiac tissue to defibrillating (stimulating) currents. Med Biol Eng Comput. 1986 Mar;24(2):130–136. doi: 10.1007/BF02443925. [DOI] [PubMed] [Google Scholar]
  33. Rattay F. Analysis of models for extracellular fiber stimulation. IEEE Trans Biomed Eng. 1989 Jul;36(7):676–682. doi: 10.1109/10.32099. [DOI] [PubMed] [Google Scholar]
  34. Roberts D. E., Scher A. M. Effect of tissue anisotropy on extracellular potential fields in canine myocardium in situ. Circ Res. 1982 Mar;50(3):342–351. doi: 10.1161/01.res.50.3.342. [DOI] [PubMed] [Google Scholar]
  35. Roth B. J., Wikswo J. P., Jr Electrical stimulation of cardiac tissue: a bidomain model with active membrane properties. IEEE Trans Biomed Eng. 1994 Mar;41(3):232–240. doi: 10.1109/10.284941. [DOI] [PubMed] [Google Scholar]
  36. Sepulveda N. G., Roth B. J., Wikswo J. P., Jr Current injection into a two-dimensional anisotropic bidomain. Biophys J. 1989 May;55(5):987–999. doi: 10.1016/S0006-3495(89)82897-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Skouibine K. B., Trayanova N. A., Moore P. K. Anode/cathode make and break phenomena in a model of defibrillation. IEEE Trans Biomed Eng. 1999 Jul;46(7):769–777. doi: 10.1109/10.771186. [DOI] [PubMed] [Google Scholar]
  38. Sobie E. A., Susil R. C., Tung L. A generalized activating function for predicting virtual electrodes in cardiac tissue. Biophys J. 1997 Sep;73(3):1410–1423. doi: 10.1016/S0006-3495(97)78173-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Spach M. S., Barr R. C. Ventricular intramural and epicardial potential distributions during ventricular activation and repolarization in the intact dog. Circ Res. 1975 Aug;37(2):243–257. doi: 10.1161/01.res.37.2.243. [DOI] [PubMed] [Google Scholar]
  40. Trayanova N. A., Roth B. J., Malden L. J. The response of a spherical heart to a uniform electric field: a bidomain analysis of cardiac stimulation. IEEE Trans Biomed Eng. 1993 Sep;40(9):899–908. doi: 10.1109/10.245611. [DOI] [PubMed] [Google Scholar]
  41. Trayanova N. Discrete versus syncytial tissue behavior in a model of cardiac stimulation--II: Results of simulation. IEEE Trans Biomed Eng. 1996 Dec;43(12):1141–1150. doi: 10.1109/10.544338. [DOI] [PubMed] [Google Scholar]
  42. Trayanova N., Skouibine K. Modeling defibrillation: effects of fiber curvature. J Electrocardiol. 1998;31 (Suppl):23–29. doi: 10.1016/s0022-0736(98)90274-6. [DOI] [PubMed] [Google Scholar]
  43. Trayanova Natalia, Skouibine Kirill, Aguel Felipe. The role of cardiac tissue structure in defibrillation. Chaos. 1998 Mar;8(1):221–233. doi: 10.1063/1.166299. [DOI] [PubMed] [Google Scholar]
  44. Tung L., Sliz N., Mulligan M. R. Influence of electrical axis of stimulation on excitation of cardiac muscle cells. Circ Res. 1991 Sep;69(3):722–730. doi: 10.1161/01.res.69.3.722. [DOI] [PubMed] [Google Scholar]
  45. Vetter F. J., McCulloch A. D. Three-dimensional analysis of regional cardiac function: a model of rabbit ventricular anatomy. Prog Biophys Mol Biol. 1998;69(2-3):157–183. doi: 10.1016/s0079-6107(98)00006-6. [DOI] [PubMed] [Google Scholar]
  46. Weidmann S. Electrical constants of trabecular muscle from mammalian heart. J Physiol. 1970 Nov;210(4):1041–1054. doi: 10.1113/jphysiol.1970.sp009256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wikswo J. P., Jr, Lin S. F., Abbas R. A. Virtual electrodes in cardiac tissue: a common mechanism for anodal and cathodal stimulation. Biophys J. 1995 Dec;69(6):2195–2210. doi: 10.1016/S0006-3495(95)80115-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zhou X., Daubert J. P., Wolf P. D., Smith W. M., Ideker R. E. Epicardial mapping of ventricular defibrillation with monophasic and biphasic shocks in dogs. Circ Res. 1993 Jan;72(1):145–160. doi: 10.1161/01.res.72.1.145. [DOI] [PubMed] [Google Scholar]
  49. Zhou X., Ideker R. E., Blitchington T. F., Smith W. M., Knisley S. B. Optical transmembrane potential measurements during defibrillation-strength shocks in perfused rabbit hearts. Circ Res. 1995 Sep;77(3):593–602. doi: 10.1161/01.res.77.3.593. [DOI] [PubMed] [Google Scholar]

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