Abstract
Short-term memory is an intrinsic property of paced cardiac myocytes that reflects the influence of pacing history, and not just the immediately preceding diastolic interval (DI), on the action potential duration (APD). Although it is recognized that short-term memory affects the dynamics of cardiac myocytes in general, and the onset of irregular cardiac rhythm in particular, its has never been adequately quantified or measured directly in experiments or numerical simulations, mainly due to the absence of appropriate techniques. As a result, very little is known about the rate- and species dependent behavior of short-term memory. In this study, we introduce a new approach that allows one to estimate how much short-term memory, M S, is present in the cardiac myocyte at different pacing rates. The new quantification is based on the fact that pacing history affects not only the APD, but the entire dynamics of paced cardiac myocytes, in particular the restitution curve. Using the patch clamp technique and numerical simulations, we measured short-term memory restitution—the dependence of M S on the cycle length—in isolated rabbit and guinea pig ventricular myocytes. In both species, M S is rate- and species-dependent, displaying a biphasic behavior as a function of cycle length. Moreover, our results indicate that there is a significant difference in M S measured between both species at small cycle lengths. Numerical simulations suggest that the kinetics of the rapidly activating delayed rectifier potassium current I Kr is partially responsible for this difference.
Similar content being viewed by others
References
Franz, M.R., Swerdlow, C.D., Liem, L.B., Schaefer J.: Cycle length dependence of human action potential duration in vivo. J. Clin. Invest. 82, 972–979 (1988)
Gilmour, R.F., Jr., Otani, N.F., Watanabe, M.: Memory and complex dynamics in canine cardiac Purkinje fibers. Am. J. Physiol. 272, H1826–H1832 (1997)
Otani, N.F., Gilmour, R.F., Jr.: Memory models for the electrical properties of local cardiac systems. J. Theor. Biol. 187, 409–436 (1997)
Watanabe, M.A., Koller, M.L.: Mathematical analysis of dynamics of cardiac memory and accommodation: theory and experiment. Am. J. Physiol. 282, H1534–H1547 (2002)
Tolkacheva, E.G., Schaeffer, D.G., Gauthier, D.J., Krassowska, W.: Condition for alternans and stability of the 1:1 response pattern in a “memory” model of paced cardiac dynamics. Phys. Rev. E. 67, 031904 (2003)
Fox, J.J., McHarg, J.L., Gilmour, R.F., Jr: Ionic mechanism of electrical alternans. Am. J. Physiol. 282, H516–30 (2003)
Cherry, E.M., Fenton, F.H.: Suppression of alternans and conduction blocks despite APD restitution: electrotonic, memory and conduction velocity effects. Am. J. Physiol. 286, H2332–2341 (2004)
Nolasco, J.B., Dahlen, D.W.: A graphic method for the study of alternation in cardiac action potentials. J. Appl. Physiol. 25, 191–196 (1968)
Guevara, M., Ward, G., Shrier, A., Glass, L.: Electrical alternans and period-doubling bifurcations. IEEE Comp. Cardiol. 562, 167 (1984)
Cherry, E.M., Fenton, F.H.: A tale of two dogs: analyzing two models of canine ventricular electrophysiology. Am. J. Physiol. 192, H43–H55 (2007)
Tolkacheva, E.G., Romeo, M.M., Guerraty, M., Gauthier, D.J.: Conditions for alternans and its control in a two-dimensional mapping model of paced cardiac dynamics. Phys. Rev. E. 69, 031904 (2004)
Kalb, S.S., Dobrovolny, H., Tolkacheva, E.G., Idriss, S.F., Krassowska, W., Gauthier, D.J.: The restitution portrait: a new method for investigating rate-dependent restitution. J. Cardiovasc. Electrophysiol. 15, 698–709 (2004)
Choi, B-P., Liu, T.L., Salama, G.S.: Adaptation of cardiac action potential durations to stimulation history with random diastolic intervals J. Cardiovasc. Electrophysiol. 15, 1188–1197 (2004)
Elharrar, V., Surawicz, B.: Cycle length effect on restitution of action potential duration in dog cardiac fibers. Am. J. Physiol. 244, H782 (1983)
Hall, G.M., Bahar, S., Gauthier, D.J.: Prevalence of rate-dependent behaviors in cardiac muscle. Phys. Rev. Lett. 82, 2995 (1999)
Tolkacheva, E.G., Anumonwo, J.M.B., Jalife, J.: The action potential duration restitution portrait of periodically paced rabbit and guinea-pig ventricular myocytes. Biophys. J. 91, 2735–2745 (2006)
Puglisi, J.L., Bers, D.M.: LabHeart: an interactive computer model of rabbit ventricular myocyte ion channels and Ca transport. Am. J. Cell Physiol. 281, C2049–C2060 (2001)
Tolkacheva, E.G., Schaeffer, D.G., Gauthier, D.J., Mitchell, C.C.: Analysis of the Fenton–Karma model through approximation by a one-dimensional map. Chaos 12, 1034–1042 (2002)
Fox, J.J., Bodenschatz, E., Gilmour, R.F., Jr.: Period-doubling instability and memory in cardiac tissue. Phys. Rev. Lett. 89, 138101–138104 (2002)
Pitruzzello, A.M., Krassowska, W., Idriss, S.F.: Spatial heterogeneity of the restitution portrait in rabbit epicardium. Am. J. Physiol. 292, H1568–1578 (2007)
Viswanathan, P.C., Shaw, R.M., Rudy, Y.: Effects of IKr and IKs heterogeneity on APD and its rate dependence. A simulation study. Circulation 99, 2466–2474 (1999)
Hua, F., Gilmour, R.F., Jr.: Contribution of IKr to rate-dependent action potential dynamics in canine endocardium. Circ. Res. 94, 810–819 (2004)
Goldhaber, J.I., Xie, L-H., Duong, T., Motter, C., Khuu, K., Weiss, J.N.: Action potential duration restitution and alternans in rabbit ventricular myocytes. The key role of intracellular calcium cycling. Circ. Res. 96, 459–466 (2005)
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tolkacheva, E.G. The Rate- and Species-Dependence of Short-Term Memory in Cardiac Myocytes. J Biol Phys 33, 35–47 (2007). https://doi.org/10.1007/s10867-007-9040-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10867-007-9040-5