Multiple traces formulation and semi-implicit scheme for modelling biological cells under electrical stimulation
ESAIM: Mathematical Modelling and Numerical Analysis , Tome 52 (2018) no. 2, pp. 659-703.

We model the electrical behavior of several biological cells under external stimuli by extending and computationally improving the multiple traces formulation introduced in Henríquez et al. [Numer. Math. 136 (2016) 101–145]. Therein, the electric potential and current for a single cell are retrieved through the coupling of boundary integral operators and non-linear ordinary differential systems of equations. Yet, the low-order discretization scheme presented becomes impractical when accounting for interactions among multiple cells. In this note, we consider multi-cellular systems and show existence and uniqueness of the resulting non-linear evolution problem in finite time. Our main tools are analytic semigroup theory along with mapping properties of boundary integral operators in Sobolev spaces. Thanks to the smoothness of cellular shapes, solutions are highly regular at a given time. Hence, spectral spatial discretization can be employed, thereby largely reducing the number of unknowns. Time-space coupling is achieved via a semi-implicit time-stepping scheme shown to be stable and second order convergent. Numerical results in two dimensions validate our claims and match observed biological behavior for the Hodgkin–Huxley dynamical model.

DOI : 10.1051/m2an/2018019
Classification : 65M38, 65M12, 65R20
Mots-clés : Multiple traces formulation, semi-implicit time stepping, biological cells, exponential convergence
Henríquez, Fernando 1 ; Jerez-Hanckes, Carlos 1

1
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Henríquez, Fernando; Jerez-Hanckes, Carlos. Multiple traces formulation and semi-implicit scheme for modelling biological cells under electrical stimulation. ESAIM: Mathematical Modelling and Numerical Analysis , Tome 52 (2018) no. 2, pp. 659-703. doi : 10.1051/m2an/2018019. http://archive.numdam.org/articles/10.1051/m2an/2018019/

[1] M. Amar, D. Andreucci, P. Bisegna and R. Gianni, A hierarchy of models for the electrical conduction in biological tissues via two-scale convergence: the nonlinear case. Differ. Integral Equ. 26 (2013) 885–912. | MR | Zbl

[2] M. Amar, D. Andreucci and R. Gianni, Asymptotic decay under nonlinear and noncoercive dissipative effects for electrical conduction in biological tissues. Nonlinear Differ. Equ. Appl. 23 (2016) 48. | DOI | MR | Zbl

[3] H. Ammari, L. Giovangigli, H. Kwon, J.K. Seo and T. Wintz, Spectroscopic conductivity imaging of a cell culture. Asymptotic Anal. 100 (2016) 87–109. | DOI | MR | Zbl

[4] H. Ammari, T. Widlak and W. Zhang, Towards monitoring critical microscopic parameters for electropermeabilization. Quart. Appl. Math. 75 (2017) 1–17. | DOI | MR | Zbl

[5] E. Anderson, Z. Bai, C. Bischof, S. Blackford, J. Dongarra, J. Du Croz, A. Greenbaum, S. Hammerling, A. Mckenney and D. Sorenson, LAPACK Users’ Guide. Vol. 9. SIAM (1999). | DOI | Zbl

[6] X. Antoine, C. Chniti and K. Ramdani, On the numerical approximation of high-frequency acoustic multiple scattering problems by circular cylinders. J. Comput. Phys. 227 (2008) 1754–1771. | DOI | MR | Zbl

[7] K. Atkinson and W. Han, Theoretical Numerical Analysis. Vol. 39. Springer (2005). | DOI | MR | Zbl

[8] M. Balabane, Boundary decomposition for Helmoltz and Maxwell equations I. Disjoint subscatterers. Asymptotic Anal. 38 (2004) 1–10. | MR | Zbl

[9] P. J. Basser and B. J. Roth, New currents in electrical stimulation of excitable tissues. Ann. Rev. Biomed. Eng. 2 (2000) 377–397. | DOI

[10] C. Bollini and F. Cacheiro, Peripheral nerve stimulation. Tech. Reg. Anesth. Pain Manag. 10 (2006) 79–88. | DOI

[11] C. Canuto and A. Quarteroni, Approximation results for orthogonal polynomials in Sobolev spaces. Math. Comput. 38 (1982) 67–86. | DOI | MR | Zbl

[12] C. Canuto, M. Y. Hussaini, A. Quarteroni and T. A. Zang, Spectral Methods. Scientific Computation. Springer-Verlag, Berlin (2006). | DOI | MR | Zbl

[13] Y. Chang and R. Harrington, A surface formulation or characteristic modes of material bodies. IEEE Trans. Antennas. Propag. 25 (1977) 789–795. | DOI

[14] D. Chapelle, A. Collin and J.-F. Gerbeau, A surface-based electrophysiology model relying on asymptotic analysis and motivated by cardiac atria modeling. Math. Models Meth. Appl. Sci. 23 (2013) 2749–2776. | DOI | MR | Zbl

[15] S. O. Choi, Y. Kim, J. W. Lee, J. H. Park, M. R. Prausnitz and M. G. Allen, Intracellular protein delivery and gene transfection by electroporation using a microneedle electrode array. Small 10 (2012) 1081–1091. | DOI

[16] X. Claeys, R. Hiptmair and C. Jerez-Hanckes, Multitrace boundary integral equations, in Direct and Inverse Problems in Wave Propagation and Applications. Vol. 14 of Radon Series on Computational and Applied Mathematics. De Gruyter, Berlin (2013) 51–100. | MR | Zbl

[17] X. Claeys, R. Hiptmair, C. Jerez-Hanckes and S. Pintarelli, Novel Multi-Trace Boundary Integral Equations for Transmission Boundary Value Problems, in Unified Transform for Boundary Value Problems: Applications and Advances, edited by A.S. Fokas and B. Pelloni. SIAM (2015) 227–258. | MR | Zbl

[18] M. Costabel, Boundary integral operators on Lipschitz domains: elementary results. SIAM J. Math. Anal. 19 (1988) 613–626. | DOI | MR | Zbl

[19] M. Costabel and E. Stephan, A direct boundary integral equation method for transmission problems. J. Math. Anal. Appl. 106 (1985) 367–413. | DOI | MR | Zbl

[20] Y. Coudiere, J. Henry and S. Labarthe, An asymptotic two-layer monodomain model of cardiac electrophysiology in the atria: derivation and convergence. SIAM J. Appl. Math. 77 (2017) 409–429. | DOI | MR | Zbl

[21] S. Doi, J. Inoue., Z. Pan and K. Tsumoto, Computational electrophysiology. Vol. 2 of Springer Series, A First Course in On Silico Medicine, Tokyo, Japan (2010). | MR | Zbl

[22] I. Dotsinsky, B. Nikolova, E. Peycheva and I. Tsoneva, New modality for electrochemotherapy of surface tumors. Biotechnol. Biotechnol. Equip. 26 (2012) 3402–3406. | DOI

[23] M. Ganesh and S. Hawkins, Simulation of acoustic scattering by multiple obstacles in three dimensions. ANZIAM J. 50 (2008) 31–45. | DOI | MR

[24] M. Ganesh and S. C. Hawkins, A high-order algorithm for multiple electromagnetic scattering in three dimensions. Numer. Algor. 50 (2009) 469–510. | DOI | MR | Zbl

[25] M. Ganesh and S. Hawkins, An efficient 𝒪 ( n ) algorithm for computing 𝒪 ( n 2 ) acoustic wave interactions in large N -obstacle three dimensional configurations. BIT Numer. Math. 55 (2015) 117–139. | DOI | MR | Zbl

[26] M. Ganesh and K. Mustapha, A fully discrete H1-Galerkin method with quadrature for nonlinear advection–diffusion–reaction equations. Numer. Algorithms 43 (2006) 355–383. | DOI | MR | Zbl

[27] D. Gottlieb and S. Orszag, Numerical analysis of spectral methods: theory and applications. Soc. Ind. Appl. Math. (1983). | Zbl

[28] A. Guittet, C. Poignard and F. Gibou, A Voronoi Interface approach to cell aggregate electropermeabilization. J. Comput. Phys. 332 (2017) 143–159. | DOI | MR | Zbl

[29] F. Henríquez, C. Jerez-Hanckes and F. Altermatt, Boundary integral formulation and semi-implicit scheme coupling for modeling cells under electrical stimulation. Numer. Math. 136 (2016) 101–145. | DOI | MR | Zbl

[30] R. Hiptmair and C. Jerez-Hanckes, Multiple traces boundary integral formulation for Helmholtz transmission problems. Adv. Comput. Math. 37 (2012) 39–91. | DOI | MR | Zbl

[31] A. Hodgkin and A. Huxley, A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117 (1952) 500–544. | DOI

[32] S. Joucla and B. Yvert, Modeling extracellular electrical neural stimulation: from basic understanding to MEA-based applications. J. Physiol. Paris 106 (2012) 146–158. | DOI

[33] S. Joucla, A. Glière and B. Yvert, Current approaches to model extracellular electrical neural microstimulation. Front. Comput. Neurosci. 8 (2014) 13. | DOI

[34] O. Kavian, M. Leguèbe, C. Poignard and L. Weynans, “Classical” electropermeabilization modeling at the cell scale. J. Math. Biol. 68 (2014) 235–265. | DOI | MR | Zbl

[35] J. Keener and J. Sneyd, Mathematical Physiology I: Cellular Physiology. Springer-Verlag, New York (1998). | DOI | MR | Zbl

[36] R. Kress, Linear Integral Equations. Vol. 82 Springer (1989). | DOI | MR | Zbl

[37] R. Kress and I. H. Sloan, On the numerical solution of a logarithmic integral equation of the first kind for the Helmholtz equation.Numer. Math. 66 (1993) 199–214. | DOI | MR | Zbl

[38] M. Leguèbe, C. Poignard and L. Weynans, A second-order Cartesian method for the simulation of electropermeabilization cell models. J. Comput. Phys. 292 (2015) 114–140. | DOI | MR | Zbl

[39] K. Lindsay, From Maxwell’s equations to the cable equation and beyond. Prog. Biophys. Mol. Biol. 85 (2004) 71–116. | DOI

[40] A. Lunardi, Analytic Semigroups and Optimal Regularity in Parabolic Problems. Springer Science & Business Media (2012). | MR | Zbl

[41] P. K. Maini, Making sense of complex phenomena in biology. Novartis Found. Symp. 247 (2002) 53–59; discussion 60–65, 84–90, 244–252. | DOI

[42] P. Martin, Multiple Scattering: Interaction of Time-Harmonic Waves with N Obstacles. Cambridge University Press (2006). | DOI | MR | Zbl

[43] H. Matano and Y. Mori, Global existence and uniqueness of a three-dimensional model of cellular electrophysiology. Discrete Contin. Dyn. Syst. 29 (2011) 1573–1636. | DOI | MR | Zbl

[44] W. Mclean, Strongly Elliptic Systems and Boundary Integral Equations. Cambridge University Press, Cambridge (2000). | MR | Zbl

[45] L. M. Mir, M. F. Bureau, J. Gehl, R. Rangara, D. Rouy, J. M. Caillaud, P. Delacre, D. Branellec, B. Schwartz and D. Scherman High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc. Nat. Acad. Sci. USA 96 (1999) 4262–4267. | DOI

[46] M. Pavlin, N. Pavselj and D. Miklavcic, Dependence of induced transmembrane potential on cell density, arrangement and cell position inside a cell system. IEEE Trans. Biomed. Eng. 40 (2002) 605–612. | DOI

[47] A. Pazy, Semigroups of Linear Operators and Applications to Partial Differential Equations. Vol. 44. Springer Science & Business Media (2012). | MR

[48] C. Pham-Dang, O. Kick, T. Collet, F. Gouin and M. Pinaud, Continuous peripheral nerve blocks with stimulating catheters. Reg. Anesth. Pain Med. 28 (2003) 83–88. | DOI

[49] A. Poggio and E. Miller, Integral equation solution of three-dimensional scattering problems, in Computer Techniques for Electromagnetics, Chap. 4, edited by R. Mittra. Pergamon, New York (1973) 159–263. | DOI

[50] T. Runst and W. Sickel. Sobolev Spaces of Fractional Order, Nemytskij Operators, and Nonlinear Partial Differential Equations. Vol. 3. Walter de Gruyter (1996). | DOI | MR | Zbl

[51] J. Saranen and G. Vainikko, Periodic Integral and Pseudodifferential Equations With Numerical Approximation. Springer Science & Business Media (2013). | MR | Zbl

[52] S. Sauter and C. Schwab. Boundary Element Methods. Springer-Verlag, Berlin, Heidelberg (2011). | DOI | MR | Zbl

[53] G. Sersa, T. Cufer, M. Cemazar, M. Rebersek and R. Zvonimir, Electrochemotherapy with bleomycin in the treatment of hypernephroma metastasis: case repeat and literature review. Tumori 86 (2000) 163–165. | DOI

[54] N. Sepulveda, J. Wikswo and D. Echt, Finite element analysis of cardiac defibrillation current distributions. IEEE Trans. Biomed. Eng. 37 (1997) 354–365. | DOI

[55] O. Steinbach, Numerical Approximation Methods for Elliptic Boundary Value Problems. Springer-Verlag, New York (2008). | DOI | MR | Zbl

[56] E. Tadmor, The exponential accuracy of Fourier and Chebyshev differencing methods. SIAM J. Numer. Anal. 23 (1986) 1–10. | DOI | MR | Zbl

[57] J. Teissié, N. Eynard, B. Gabriel and M. Rols, Electropermeabilization of cell membranes. Adv. Drug Deliv. Rev. 35 (1999) 3–19. | DOI

[58] V. Thomée. Galerkin finite element methods for parabolic problems, in Springer Series in Computational Mathematics (2006). | MR | Zbl

[59] N. Trayanova, J. Constantino, T. Ashihara and G. Plank, Modeling defibrillation of the heart: approaches and insights. IEEE Rev. Biomed. Eng. 4 (2012) 89–102. | DOI

[60] U. Van Rienen, U. Schreiber, S. Schulze, U. Gimsa, W. Baumann, D. Weiss, J. Gimsa, R. Benecke and H.W. Pau, Electro-quasistatic simulations in bio-systems engineering and medical engineering. Adv. Radio Sci. 3 (2005) 39–49. | DOI

[61] P. Waterman, Matrix formulation of electromagnetic scattering. Proc. of IEEE 53 (1965) 805–812. | DOI | Zbl

[62] T.-K. Wu and L. L. Tsai, Scattering from arbitrarily-shaped lossy dielectric bodies of revolution. Radio Sci. 12 (1977) 709–718. | DOI

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