Skip to main content

Nonlinear dynamics of two-dimensional cardiac action potential duration mapping model with memory

Abstract

The aim of this work is the analysis of the nonlinear dynamics of two-dimensional mapping model of cardiac action potential duration (2D-map APD) with memory derived from one dimensional map (1D-map). Action potential duration (APD) restitution, which relates APD to the preceding diastolic interval (DI), is a useful tool for predicting cardiac arrhythmias. For a constant rate of stimulation the short action potential during alternans is followed by a longer DI and inversely. It has been suggested that these differences in DI are responsible for the occurrence and maintenance of APD alternans. We focus our attention on the observed bifurcations produced by a change in the stimulation period and a fixed value of a particular parameter in the model. This parameter provides new information about the dynamics of the APD with memory, such as the occurrence of bistabilities not previously described in the literature, as well as the fact that synchronization rhythms occur in different ways and in a new fashion as the stimulation frequency increases. Moreover, we show that this model is flexible enough as to accurately reflect the chaotic dynamics properties of the APD: we have highlighted the fractal structure of the strange attractor of the 2D-map APD, and we have characterized chaos by tools such as the calculation of the Lyapunov exponents, the fractal dimension and the Kolmogorov entropy, with the next objective of refining the study of the nonlinear dynamics of the duration of the action potential and to apply methods of controlling chaos.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

References

  • Babloyantz A, Destexhe A (1988) Is the normal heart a periodic oscillator. Biol Cybern 58:203–211

    MathSciNet  Article  Google Scholar 

  • Bergé P, Pomeau Y, Vidal C (1984) L’ordre dans le chaos. Hermann, Paris

    MATH  Google Scholar 

  • Bittihn P, Berg S, Parlitz U, Luther S (2017) Emergent dynamics of spatio-temporal chaos in a heterogeneous excitable medium. Chaos Interdiscip J Nonlinear Sci 27(9):093,931. https://doi.org/10.1063/1.4999604

    MathSciNet  Article  Google Scholar 

  • Cain JW (2007) Criterion for stable reentry in a ring of cardiac tissue. J Math Biol 55

  • Chatterjee K, Harris A, Davies J et al (1969) T-wave changes after artificial pacing. Lancet 1:759–760

    Article  Google Scholar 

  • Cherubini C et al (2017) A note on stress-driven anisotropic diffusion and its role in active deformable media. J Theor Biol 430:221–228

    Article  MATH  Google Scholar 

  • Chialvo D, Jalife J (1987) Low dimensional chaos in cardiac tissue. Nature 330:749–752

    Article  Google Scholar 

  • Ding M, Grebogi C, Ott E, Sauer T, Yorke J (1993) Estimating correlation dimension from a chaotic time series: When does plateau onset occur? Physica D 69:404–424

    MathSciNet  Article  MATH  Google Scholar 

  • Ditto WL, Rauseo SN, Spano ML (1990) Experimental control of chaos. Phys Rev Lett 65:3211–3214. https://doi.org/10.1103/PhysRevLett.65.3211

    Article  Google Scholar 

  • Eckmann J (1981) Roads to turbulence in dissipative dynamical systems. Rev Mod Phys 53:643–654. https://doi.org/10.1103/RevModPhys.53.643

    MathSciNet  Article  MATH  Google Scholar 

  • Eyebe Fouda J, Koepf W, Jacquir S (2017) The ordinal Kolmogorov–Sinai entropy: a generalized approximation. Commun Nonlinear Sci Numer Simul 46:103–115

    MathSciNet  Article  Google Scholar 

  • Fenton F, Karma A (1998) Vortex dynamics in three-dimensional continuous myocardium with fiber rotation: filament instability and fibrillation. Chaos Interdiscip J Nonlinear Sci 8(1):20–47. https://doi.org/10.1063/1.166311

    Article  MATH  Google Scholar 

  • Fenton F, Gizzi A, Cherubini C, Pomella N, Filippi S (2013) Role of temperature on nonlinear cardiac dynamics. Phys Rev E 87(042):717. https://doi.org/10.1103/PhysRevE.87.042717

    Google Scholar 

  • Fleetwood D, Masden J, Giordano N (1983) 1/f noise in platinum films and ultrathin platinum wires: evidence for a common bulk origin. Phys Rev Lett 50:450–453

    Article  Google Scholar 

  • Frigg R (2004) Kolmogorov–Sinai, entropy a measure for chaotic behaviour? Bridging the gap between dynamical systems theory and communication theory. Br J Philos Sci 55:411–434

    MathSciNet  Article  MATH  Google Scholar 

  • Garfinkel A, Spano M, Ditto W, Weiss J (1992) Controlling cardiac chaos. Science 257:1230–1235

    Article  Google Scholar 

  • Garzón A, Grigoriev R (2017) Memory effects, transient growth, and wave breakup in a model of paced atrium. Chaos Interdiscip J Nonlinear Sci 27(9):093,917. https://doi.org/10.1063/1.4999601

  • Garzón A, Grigoriev R, Fenton F (2009) Model-based control of cardiac alternans on a ring. Phys Rev E 80(021):932. https://doi.org/10.1103/PhysRevE.80.021932

    Google Scholar 

  • Garzón A, Grigoriev R, Fenton F (2011) Model-based control of cardiac alternans in purkinje fibers. Phys Rev E 84(041):927. https://doi.org/10.1103/PhysRevE.84.041927

    Google Scholar 

  • Garzón A, Grigoriev R, Fenton F (2014) Continuous-time control of alternans in long purkinje fibers. Chaos Interdiscip J Nonlinear Sci 24(3):033,124. https://doi.org/10.1063/1.4893295

  • Gizzi A, Cherry EM, Gilmour R, Luther S, Filippi S, Fenton F (2013) Effects of pacing site and stimulation history on alternans dynamics and the development of complex spatiotemporal patterns in cardiac tissue. Front Physiol 4(71)

  • Gizzi A, Loppini A, Ruiz-Baier R, Ippolito A, Camassa A, La Camera A, Emmi E, Di Perna L, Garofalo V, Cherubini C, Filippi S (2017) Nonlinear diffusion and thermo-electric coupling in a two-variable model of cardiac action potential. Chaos Interdiscip J Nonlinear Sci 27(9):093,919. https://doi.org/10.1063/1.4999610

  • Glass L, Guevara M, Shrier A, Perez R (1983) Bifurcation and chaos in a periodically stimulated cardiac oscillator. Physica D 7(1):89–101

    Article  Google Scholar 

  • Grebogi C, Ott E, Yorke J (1987) Chaos, strange attractors and fractal basin boundaries in nonlinear dynamics. Science 238:632–638

    MathSciNet  Article  MATH  Google Scholar 

  • Guevara M (1997) Concepts and techniques in bioelectric measurements: Is the medium carrying the message? edited by J Billette and AR Leblanc Editions de l’Ecole polythenique de Montreal 7:67–87

  • Guevara MR (1988) Spatiotemporal patterns of block in an ionic model of cardiac purkinje fibre. In: Markus M, Müller SC, Nicolis G (eds) From chemical to biological organization. Springer, Heidelberg, pp 273–281

    Chapter  Google Scholar 

  • Guevara M, Glass L, Shrier A (1981) Phaselocking, period-doubling bifurcations, and irregular dynamics inperiodically stimulated cardiac cells. Science 214(4527):1350–1353. https://doi.org/10.1126/science.7313693. http://science.sciencemag.org/content/214/4527/1350. http://science.sciencemag.org/content/214/4527/1350.full.pdf

  • Guevara M, Ward G, Shrier A, Glass L (1984) Electrical alternans and period doubling bifurcations. In: IEEE Computers in Cardiology pp 167–170

  • Guevara M, Alonso F, Jeandupeux D, Vanginneken A (1989) Alternans in periodically stimulated isolated ventricular myocytes: experiment and model. In: Cell to cell signalling: from experiment to theoretical model pp 551–563

  • Guevara M, Shrier A, Orlowski J, Glass L (2016) George Ralph mines (1886–1914): the dawn of cardiac nonlinear dynamics. J Physiol 594(9):2361–2371

    Article  Google Scholar 

  • Hescheler J, Speicher R (1989) Regular and chaotic behaviour of cardiac cells stimulated at frequencies between 2 and 20 Hz. Eur Biophys J 17:273–280

    Article  Google Scholar 

  • Hilborn RC (2000) Chaos and nonlinear dynamics: an introduction for scientists and engineers

  • Hoekstra B, Diks C, Allessie M, Goedb J (1995) Nonlinear analysis of epicardial atrial electrograms of electrically induced atrial fibrillation in man. J Cardiovasc Electrophysiol 6(6):419–440. https://doi.org/10.1111/j.1540-8167.1995.tb00416.x

    Article  Google Scholar 

  • Jensen J et al (1984) Chaos in the Beeler-Reuter system for the action potential of ventricular myocardial fibres. Physica D 13(1):269–277. https://doi.org/10.1016/0167-2789(84)90283-5

    MathSciNet  Article  MATH  Google Scholar 

  • Karmakar C, Udhayakumar R, Palaniswami M (2015) Distribution entropy (disten): a complexity measure to detect arrhythmia from short length rr interval time series. In: 37th Annual international conference of the IEEE Engineering in Medicine and Biology Society (EMBC), pp 5207–5210

  • Kesmia M, Boughaba S, Jacquir S (2016) Predictive chaos control for the 1d-map of action potential duration. Chaotic Model Simul J 3:387–398

    Google Scholar 

  • Kesmia M, Boughaba S, Jacquir S (2018a) Control of irregular cardiac rhythm. Chaotic Model Simul J 1:91–99

    MATH  Google Scholar 

  • Kesmia M, Boughaba S, Jacquir S (2018b) New approach of controlling cardiac alternans. Discrete Contin Dyn Syst B 23(2):975–989

    MathSciNet  Article  MATH  Google Scholar 

  • King C (1991) Fractal and chaotic dynamics in nervous systems. Prog Neurobiol 36(4):279–308

    Article  Google Scholar 

  • Kolmogorov A (1959) Entropy per unit time as a metric invariant of automorphism. Doklady Russ Acad Sci 124:754–755

    MathSciNet  MATH  Google Scholar 

  • Krogh-Madsen T, Kold Taylor L, Skriver A, Schaffer P, Guevara M (2017) Regularity of beating of small clusters of embryonic chick ventricular heart-cells: experiment versus stochastic single-channel population model. Chaos Interdiscip J Nonlinear Sci 27(9):093,929. https://doi.org/10.1063/1.5001200

  • Landaw J, Garfinkel A, Weiss J, Qu Z (2017) Memory-induced chaos in cardiac excitation. Phys Rev Lett 118(138):101. https://doi.org/10.1103/PhysRevLett.118.138101

    Google Scholar 

  • Lee K et al (2009) Effect of short-term cardiac memory on ventricular electrical restitution and qt intervals in humans. Kaohsiung J Med Sci 25(2):53–61

    Article  Google Scholar 

  • Lee K, Chu C, Lin T et al (2008) Effect of sodium and calcium channel blockers on short-term cardiac memory in humans. Int J Cardiol 123(2):94–101

    Article  Google Scholar 

  • Lewis T, Guevara M (1990) Chaotic dynamics in an ionic model of the propagated cardiac action potential. J Theor Biol 146(3):407–432

    Article  Google Scholar 

  • Luther ea (2011) Low-energy control of electrical turbulence in the heart. Nature 475:235

  • Mayordomo E, Kolmogorov A (2002) Complexity characterization of constructive Hausdorff dimension. Inf Process Lett 84:1–3

    MathSciNet  Article  MATH  Google Scholar 

  • Morgan SW, Biktasheva IV, Biktashev VN (2008) Control of scroll-wave turbulence using resonant perturbations. Phys Rev E 78(046):207. https://doi.org/10.1103/PhysRevE.78.046207

    MathSciNet  Google Scholar 

  • Nagaiah C, Kunisch K, Plank G (2013) Optimal control approach to termination of re-entry waves in cardiac electrophysiology. J Math Biol 67:359–388

    MathSciNet  Article  MATH  Google Scholar 

  • Ohnishi M, Inaba N (1994) A singular bifurcation into instant chaos in a piecewise-linear circuit. IEEE Trans Circuits Syst 41:433–442

    MathSciNet  Article  Google Scholar 

  • Oida E, Moritani T, Yamori Y (1997) Tone-entropy analysis on cardiac recovery after dynamic exercise. J Appl Physiol 82(6):1794–1801. https://doi.org/10.1152/jappl.1997.82.6.1794 (pMID: 9173943)

    Article  Google Scholar 

  • Otani N (2017) Theory of the development of alternans in the heart during controlled diastolic interval pacing. Chaos Interdiscip J Nonlinear Sci 27(9):093,935. https://doi.org/10.1063/1.5003250

  • Otani N, Gilmour R (1997) Memory models for the properties of local cardiac systems. J Theor Biol 187:409–436

    Article  Google Scholar 

  • Pincus S, Viscarello R (1992) Approximate entropy: a regularity measure for fetal heart rate analysis. Obstet Gynecol 79:249–255

    Google Scholar 

  • Pumir A, Nikolski V, Hörning M, Isomura A, Agladze K, Yoshikawa K, Gilmour R, Bodenschatz E, Krinsky V (2007) Wave emission from heterogeneities opens a way to controlling chaos in the heart. Phys Rev Lett 99(208):101. https://doi.org/10.1103/PhysRevLett.99.208101

    Google Scholar 

  • Rappel W, Fenton F, Karma A (1999) Spatiotemporal control of wave instabilities in cardiac tissue. Phys Rev Lett 83

  • Rosenbaum M, Blanco H, Elizari M et al (1982) Electrotonic modulation of the t wave and cardiac memory. Am J Cardiol 50(2):213–222

    Article  Google Scholar 

  • Ryan S et al (1994) Gender- and age-related differences in heart rate dynamics: Are women more complex than men? J Am Coll Cardiol 24(7):1700–1707

    Article  Google Scholar 

  • Schuster HG (1988) Deterministic chaos: an introduction (2nd revised edition)

  • Shilnikov L (1981) The bifurcation theory and quasi-hyperbiloc attractors. Uspehi Mat Nauk 36:240–241

    Google Scholar 

  • Sinai Y (1959) On the notion of entropy of a dynamical system. Doklady Russ Acad Sci 124:768–771

    MathSciNet  MATH  Google Scholar 

  • Smith J, Cohen R (1984) Simple finite-element model accounts for wide range of cardiac dysrhythmias. Proceedings of the National Academy of Sciences 81(1):233–237. https://doi.org/10.1073/pnas.81.1.233. http://www.pnas.org/content/81/1/233. http://www.pnas.org/content/81/1/233.full.pdf

  • Sprott J, Rowlands G (1995) Chaos data analyzer: the professional version. Physics Academic Software, Raleigh

    Google Scholar 

  • Tolkacheva E, Schaeffer D, Gauthier D, Mitchell C (2002) Analysis of the fentonkarma model through an approximation by a one-dimensional map. Chaos Interdiscip J Nonlinear Sci 12(4):1034–1042. https://doi.org/10.1063/1.1515170

    Article  MATH  Google Scholar 

  • Voss A, Schulz S, Schroeder R, Baumert M, Caminal P(2009) Methods derived from nonlinear dynamics for analysing heart rate variability. Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 367(1887):277–296. https://doi.org/10.1098/rsta.2008.0232.http://rsta.royalsocietypublishing.org/content/367/1887/277. http://rsta.royalsocietypublishing.org/content/367/1887/277.full.pdf

  • Wei N, Mori Y, Tolkacheva E (2015) The role of short term memory and conduction velocity restitution in alternans formation. J Theor Biol 367:21–28

    MathSciNet  Article  Google Scholar 

  • Wessel N, Schumann A, Schirdewan A, Voss A, Kurths J (2000) Entropy measures in heart rate variability data. In: Brause RW, Hanisch E (eds) Medical data analysis. Springer, Heidelberg, pp 78–87

    Chapter  Google Scholar 

  • Wu R, Patwardhan A (2004) Restitution of action potential duration during sequential changes in diastolic intervals shows multimodal behavior. Circ Res 94(5):634–641. https://doi.org/10.1161/01.RES.0000119322.87051.A9

    Article  Google Scholar 

  • Xu B, Jacquir S, Laurent G, Bilbault J, Binczak S (2011) A hybrid stimulation strategy for suppression of spiral waves in cardiac tissue. Chaos Solitons Fractals 44(8):633–639

    Article  Google Scholar 

  • Xu B, Jacquir S, Laurent G, Binczak S, Pont O, Yahia H (2015) In vitro arrhythmia generation by mild hypothermia: a pitchfork bifurcation type process. Physiol Meas 36(3):579. http://stacks.iop.org/0967-3334/36/i=3/a=579

  • Yehia A, Jeandupeux D, Alonso F, Guevara M (1999) Hysteresis and bistability in the direct transition from 1:1 to 2:1 rhythm in periodically driven single ventricular cells. Chaos Interdiscip J Nonlinear Sci 9(4):916–931. https://doi.org/10.1063/1.166465

    Article  MATH  Google Scholar 

  • Yentes J, Hunt N, Schmid K, Kaipust J, McGrath D, Stergiou N (2013) The appropriate use of approximate entropy and sample entropy with short data sets. Ann Biomed Eng 41(2):349–365

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Professor Michael R. Guevara (Department of Physiology and Centre for Nonlinear Dynamics in Physiology and Medicine, McGill University, Montreal, Quebec) for his insightful comments and helpful suggestions, which have helped improve the quality and presentation of the paper significantly.

Author information

Affiliations

Authors

Corresponding author

Correspondence to S. Jacquir.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kesmia, M., Boughaba, S. & Jacquir, S. Nonlinear dynamics of two-dimensional cardiac action potential duration mapping model with memory. J. Math. Biol. 78, 1529–1552 (2019). https://doi.org/10.1007/s00285-018-1318-7

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00285-018-1318-7

Keywords

  • Cardiac action potential duration
  • Memory
  • Bifurcation
  • Periodic dynamics
  • Fixed point
  • Strange attractor
  • Fractal structure
  • Chaos

Mathematics Subject Classification

  • 37D45
  • 37N25
  • 92C50
  • 92B25
  • 93C10
  • 93C55