Abstract
Discharges of different epilepsies are characterized by different signal shape and duration. The authors adhere to the hypothesis that spike-wave discharges are long transient processes rather than attractors. This helps to explain some experimentally observed properties of discharges, including the absence of a special termination mechanism and quasi-regularity. Analytical approaches mostly cannot be applied to studying transient dynamics in large networks. Therefore, to test the observed phenomena for universality one has to show that the same results can be achieved using different model types for nodes and different connectivity terms. Here, we study a class of simple network models of a thalamocortical system and show that for the same connectivity matrices long, but finite in time quasi-regular processes mimicking epileptic spike-wave discharges can be found using nodes described by three neuron models: FitzHugh – Nagumo, Morris – Lecar and Hodgkin – Huxley. This result takes place both for linear and nonlinear sigmoid coupling.
REFERENCES
van Ooytien, A., van Pelt, J., Corner, M. A., and da Silva, F. H., The Emergence of Long-Lasting Transients of Activity in Simple Neural Networks, Biol. Cybern., 1992, vol. 67, no. 3, pp. 269–277.
Riecke, H., Roxin, A., Madruga, S., and Solla, S. A., Multiple Attractors, Long Chaotic Transients, and Failure in Small-World Networks of Excitable Neurons, Chaos, 2007, vol. 17, no. 2, 026110, 15 pp.
Sysoev, I. V., Ponomarenko, V. I., and Prokhorov, M. D., Reconstruction of Ensembles of Nonlinear Neurooscillators with Sigmoid Coupling Function, Nonlinear Dyn., 2019, vol. 95, no. 3, pp. 2103–2116.
Afraimovich, V. S., Rabinovich, M. I., and Varona, P., Heteroclinic Contours in Neural Ensembles and the Winnerless Competition Principle, Internat. J. Bifur. Chaos Appl. Sci. Engrg., 2004, vol. 14, no. 4, pp. 1195–1208.
Afraimovich, V., Tristan, I., Varona, P., and Rabinovich, M., Transient Dynamics in Complex Systems: Heteroclinic Sequences with Multidimensional Unstable Manifolds, Discontinuity Nonlinearity Complex., 2013, vol. 2, no. 1, pp. 21–41.
Perez Velazquez, J. L., Cortez, M. A., Carter Snead, O. III, and Wennberg, R., Dynamical Regimes Underlying Epileptiform Events: Role of Instabilities and Bifurcations in Brain Activity, Phys. D, 2003, vol. 186, no. 3–4, pp. 205–220.
Marten, F., Rodrigues, S., Benjamin, O., Richardson, M. P., and Terry, J. R., Onset of Polyspike Complexes in a Mean-Field Model of Human Electroencephalography and Its Application to Absence Epilepsy, Philos. Trans. R. Soc. Lond. Ser. A Math. Phys. Eng. Sci., 2009, vol. 367, no. 1891, pp. 1145–1161.
Suffczynski, P., Kalitzin, S., and Lopes Da Silva, F. H., Dynamics of Non-Convulsive Epileptic Phenomena Modeled by a Bistable Neuronal Network, Neuroscience, 2004, vol. 126, no. 2, pp. 467–484.
Lytton, W., Computer Modelling of Epilepsy, Nat. Rev. Neurosci., 2008, vol. 9, no. 8, pp. 626–637.
El Houssaini, K., Bernard, Ch., and Jirsa, V. K., The Epileptor Model: A Systematic Mathematical Analysis Linked to the Dynamics of Seizures, Refractory Status Epilepticus, and Depolarization Block, eNeuro, 2020, vol. 7, no. 2, 54 pp.
Rabinovich, M. I., Zaks, M. A., and Varona, P., Sequential Dynamics of Complex Networks in Mind: Consciousness and Creativity, Phys. Rep. 2020, vol. 883, pp. 1–32.
Kapustnikov, A. A., Sysoeva, M. V., and Sysoev, I. V., Modeling Spike-Wave Discharges in the Brain with Small Neurooscillator Networks, Mat. Biolog. Bioinform., 2020, vol. 15, no. 2, pp. 138–147 (Russian).
Lüttjohann, A. and van Luijtelaar, G., The Dynamics of Cortico-Thalamo-Cortical Interactions at the Transition from Pre-Ictal to Ictal LFPs in Absence Epilepsy, Neurobiol. Dis., 2012, vol. 47, no. 1, pp. 47–60.
Sysoeva, M. V., Lüttjohann, A., van Luijtelaar, G., and Sysoev, I. V., Dynamics of Directional Coupling Underlying Spike-Wave Discharges, Neuroscience, 2016, vol. 314, pp. 75–89.
Marescaux, C., Vergnes, M., and Depaulis, A., Genetic Absence Epilepsy in Rats from Strasbourg: A Review, J. Neural. Transm. Suppl., 1992, vol. 35, pp. 37–69.
Coenen, A. M. L. and van Luijtelaar, G., Genetic Animal Models for Absence Epilepsy: A Review of the WAG/Rij Strain of Rats, Behav. Genet., 2003, vol. 33, no. 6, pp. 635–655.
Taylor, P. N., Wang, Y., Goodfellow, M., Dauwels, J., Moeller, F., Stephani, U., and Baier, G., A Computational Study of Stimulus Driven Epileptic Seizure Abatement, PLoS One, 2014, vol. 9, no. 12, e114316, 26 pp.
Proske, J. H., Jeanmonod, D., and Verschure, P. F., A Computational Model of Thalamocortical Dysrhythmia, Eur. J. Neurosci., 2011, vol. 33, no. 7, pp. 1281–1290.
Medvedeva, T. M., Sysoeva, M. V., van Luijtelaar, G., and Sysoev, I. V., Modeling Spike-Wave Discharges by a Complex Network of Neuronal Oscillators, Neural Netw., 2018, vol. 98, pp. 271–282.
Medvedeva, T. M., Sysoeva, M. V., Lüttjohann, A., van Luijtelaar, G., and Sysoev, I. V., Dynamical Mesoscale Model of Absence Seizures in Genetic Models, PLoS One, 2020, vol. 15, no. 9, e0239125, 23 pp.
Kapustnikov, A. A., Sysoeva, M. V., and Sysoev, I. V., Transient Dynamics in a Class of Mathematical Models of Epileptic Seizures, Commun. Nonlinear Sci. Numer. Simul. 2022, vol. 109, Paper No. 106284, 9 pp.
Meeren, H. K. M., Pijn, J. P., Van Luijtelaar, E. L. J. M., Coenen, A. M. L., and Lopes da Silva, F. H., Cortical Focus Drives Widespread Corticothalamic Networks during Spontaneous Absence Seizures in rats, J. Neurosci., 2002, vol. 22, no. 4, pp. 1480–1495.
Grishchenko, A. A., van Rijn, C. M., and Sysoev, I. V., Comparative Analysis of Methods for Estimation of Undirected Coupling from Time Series of Intracranial EEGs of Cortex of Rats-Genetic Models of Absence Epilepsy, Mat. Biolog. Bioinform., 2017, vol. 12, no. 2, pp. 317–326.
Badawy, R. A., Harvey, A. S., and Macdonell, R. A., Cortical Hyperexcitability and Epileptogenesis: Understanding the Mechanisms of Epilepsy: Part 1, J. Clin. Neurosci., 2009, vol. 16, no. 3, pp. 355–365.
Badawy, R. A., Harvey, A. S., and Macdonell, R. A., Cortical Hyperexcitability and Epileptogenesis: Understanding the Mechanisms of Epilepsy: Part 2, J. Clin. Neurosci., 2009, vol. 16, no. 4, pp. 485–500.
Spencer, S. S., Neural Networks in Human Epilepsy: Evidence Of and Implications for Treatment, Epilepsia, 2002, vol. 43, no. 3, pp. 219–227.
FitzHugh, R., Impulses and Physiological States in Theoretical Models of Nerve Membrane, Biophys. J., 1961, vol. 1, no. 6, pp. 445–466.
Nagumo, J., Arimoto, S., and Yoshizawa, S., An Active Pulse Transmission Line Simulating Nerve Axon, Proc. of the IRE, 1962, vol. 50, no. 10, pp. 2061–2070.
Morris, C. and Lecar, H., Voltage Oscillations in the Barnacle Giant Muscle Fiber, Biophys. J., 1981, vol. 35, no. 1, pp. 193–213.
Hodgkin, A. L. and Huxley, A. F., A Quantitative Description of Membrane Current and Its Application to Conduction and Excitation in Nerve, J. Physiol., 1952, vol. 114, no. 4, pp. 500–544.
Gerster, M., Berner, R., Sawicki, J., Zakharova, A., Škoch, A., Hlinka, J., Lehnertz, K., and Schöll, E., FitzHugh – Nagumo Oscillators on Complex Networks Mimic Epileptic-Seizure-Related Synchronization Phenomena, Chaos, 2020, vol. 30, no. 12, 123130, 12 pp.
Estarellas, C., Masoliver, M., Masoller, C., and Mirasso, C. R., Characterizing Signal Encoding and Transmission in Class I and Class II Neurons via Ordinal Time-Series Analysis, Chaos, 2020, vol. 30, no. 1, 013123, 15 pp.
Kopell, N., Ermentrout, G. B., Whittington, M. A., and Traub, R. D., Gamma Rhythms and Beta Rhythms Have Different Synchronization Properties, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 4, pp. 1867–1872.
Marreiros, A. C., Daunizeau, J., Kiebel, S. J., and Friston, K. J., Population Dynamics: Variance and the Sigmoid Activation Function, Neuroimage, 2008, vol. 42, no. 1, pp. 147–157.
Dahlem, M. A., Hiller, G., Panchuk, A., and Schöll, E., Dynamics of Delay-Coupled Excitable Neural Systems, Internat. J. Bifur. Chaos Appl. Sci. Engrg., 2009, vol. 19, no. 2, pp. 745–753.
Egorov, N. M., Ponomarenko, V. I., Sysoev, I. V., and Sysoeva, M. V., Simulation of Epileptiform Activity Using Network of Neuron-Like Radio Technical Oscillators, Tech. Phys., 2021, vol. 66, no. 3, pp. 505–514; see also: Zh. Tekh. Fiz., 2021, vol. 91, no. 3, pp. 519-528.
Egorov, N. M., Kulminskiy, D. D., Sysoev, I. V., Ponomarenko, V. I., and Sysoeva, M. V., Transient Dynamics in Electronic Neuron-Like Circuits in Application to Modeling Epileptic Seizures, Nonlinear Dyn., 2022, vol. 108, no. 4, pp. 4231–4242.
Izhikevich, E. M., Which Model to Use for Cortical Spiking Neurons?, IEEE Trans. Neural Netw., 2004, vol. 15, no. 5, pp. 1063–1070.
Dmitrichev, A. S., Kasatkin, D. V., Klinshov, V. V., Kirillov, S. Yu., Maslennikov, O. V., Shchapin, D. S., and Nekorkin, V. I., Nonlinear Dynamical Models of Neurons: Review, Izv. Vyssh. Uchebn. Zaved. Prikl. Nelin. Dinam., 2018, vol. 26, no. 4, pp. 5–58 (Russian).
Lenkov, D. N., Volnova, A. B., Pope, A. R. D., and Tsytsarev, V., Advantages and Limitations of Brain Imaging Methods in the Research of Absence Epilepsy in Humans and Animal Models, J. Neurosci. Methods, 2013, vol. 212, no. 2, pp. 195–202.
Izhikevich, E. M. and Edelman, G. M., Large-Scale Model of Mammalian Thalamocortical Systems, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, no. 9, pp. 3593–3598.
Ching, Sh., Cimenser, A., Purdon, P. L., Brown, E. N., and Kopell, N. J., Thalamocortical Model for a Propofol-Induced \(\alpha\)-Rhythm Associated with Loss of Consciousness, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 52, pp. 22665–22670.
Sompolinsky, H., Crisanti, A., and Sommers, H.-J., Chaos in Random Neural Networks, Phys. Rev. Lett., 1988, vol. 61, no. 3, pp. 259–262.
Kadmon, J. and Sompolinsky, H., Transition to Chaos in Random Neuronal Networks, Phys. Rev. X, 2015, vol. 5, no. 4, 041030, 28 pp.
Lüttjohann, A. and Pape, H. C., Regional Specificity of Cortico-Thalamic Coupling Strength and Directionality during Waxing and Waning of Spike and Wave Discharges, Sci. Rep., 2019, vol. 9, no. 1, 2100, 11 pp.
Hindmarsh, J. L. and Rose, R. M., A Model of Neuronal Bursting Using Three Coupled First Order Differential Equations, Proc. R. Soc. Lond. Ser. B Biol. Sci., 1984, vol. 221, no. 1222, pp. 87–102.
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This research was funded by the Russian Science Foundation, Grant No. 19-72-10030-P https://rscf.ru/project/19-72-10030/.
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MSC2010
: 34C10, 37N25, 92-08
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Kapustnikov, A.A., Sysoeva, M.V. & Sysoev, I.V. Universal Transient Dynamics in Oscillatory Network Models of Epileptic Seizures. Regul. Chaot. Dyn. 29, 190–204 (2024). https://doi.org/10.1134/S156035472401012X
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DOI: https://doi.org/10.1134/S156035472401012X