Skip to main content
SpringerLink
Log in

The Early Phases of Epileptogenesis Induced by Status Epilepticus Are Characterized by Persistent Dynamical Regime of Intermittency Type

  • Conference paper
  • First Online:
Recurrence Plots and Their Quantifications: Expanding Horizons

Part of the book series: Springer Proceedings in Physics ((SPPHY,volume 180))

Abstract

Pre-clinical studies aimed to test potential anti-epileptogenic therapies by using the animal models of epileptogenesis induced by status epilepticus (SE), highlighted that the early days following the end of this primary insult represent a crucial temporal window for the subsequent development of epilepsy. In this study, we characterized the EEG dynamics during such crucial period of epileptogenesis, according to the conceptual framework of nonlinear dynamical systems. To this aim, we analyzed by recurrence quantification analysis (RQA) the EEG signals associated to the early days of epileptogenesis induced by SE in rodents according to two well-known experimental protocols, i.e., (i) SE induced by electrical stimulation of the hippocampus in rats (n = 7) and (ii) SE induced by the intra-amygdala administration of kainic-acid in mice (n = 6). We show that the EEG signals during the early 1–2 days post-SE are characterized by an enhanced and persistent rate of occurrence of dynamical regimes of intermittency type. This finding is common to both models of SE, hence it could represent the dynamical hallmark of pro-epileptogenic insults and could correlate with the efficacy of such insults to promote functional changes leading to the development of epilepsy. Future works aimed to deepen our findings could lead to the identification of a potential prognostic factor of the development of epilepsy as well as improve the portability of pre-clinical studies aimed to target new potential therapeutics designed to prevent the development of epilepsy.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. A. Pitkänen, K. Lukasiuk, Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epil. Behav. 14(1), 16–25 (2009)

    Article  Google Scholar 

  2. A. Pitkänen, K. Lukasiuk, Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol. 10(2), 173–186 (2011)

    Article  Google Scholar 

  3. C.L. Webber, J.P. Zbilut, Dynamical assessment of physiological systems and states using recurrence plot strategies. J. Appl. Physiol. 76(2), 965–973 (1994)

    Google Scholar 

  4. J.P. Zbilut, A. Giuliani, C.L. Webber, Detecting deterministic signals in exceptionally noisy environments using cross-recurrence quantification. Phys. Lett. A 246(1), 122–128 (1998)

    Article  ADS  Google Scholar 

  5. J.P. Zbilut, A. Giuliani, C.L. Webber, Recurrence quantification analysis as an empirical test to distinguish relatively short deterministic versus random number series. Phys. Lett. A 267(2), 174–178 (2000)

    Article  ADS  Google Scholar 

  6. W. Löscher, C. Brandt, Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol. Rev. 62(4), 668–700 (2010)

    Article  Google Scholar 

  7. A. Pitkänen, Therapeutic approaches to epileptogenesis—hope on the horizon. Epilepsia 51(s3), 2–17 (2010)

    Article  Google Scholar 

  8. D.H. Lowenstein, B.K. Alldredge, Status epilepticus. N. Engl. J. Med. 338(14), 970–976 (1998)

    Article  Google Scholar 

  9. A. Pitkänen, I. Kharatishvili, S. Narkilahti, K. Lukasiuk, J. Nissinen, Administration of diazepam during status epilepticus reduces development and severity of epilepsy in rat. Epil. Res. 63(1), 27–42 (2005)

    Article  Google Scholar 

  10. M.J. Lehmkuhle, K.E. Thomson, P. Scheerlinck, W. Pouliot, B. Greger, F.E. Dudek, A simple quantitative method for analyzing electrographic status epilepticus in rats. J. Neurophysiol. 101(3), 1660–1670 (2009)

    Article  Google Scholar 

  11. M.G. De Simoni, C. Perego, T. Ravizza, D. Moneta, M. Conti, F. Marchesi, A. De Luigi, S. Garattini, A. Vezzani, Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur. J. Neurosci. 12(7), 2623–2633 (2000)

    Article  Google Scholar 

  12. F. Noè, A.H. Pool, J. Nissinen, M. Gobbi, R. Bland, M. Rizzi, C. Balducci, F. Ferraguti, G. Sperk, M.J. During, A. Pitkänen, A. Vezzani, Neuropeptide Y gene therapy decreases chronic spontaneous seizures in a rat model of temporal lobe epilepsy. Brain 131(6), 1506–1515 (2008)

    Article  Google Scholar 

  13. G. Mouri, E. Jimenez-Mateos, T. Engel, M. Dunleavy, S. Hatazaki, A. Paucard, S. Matsushima, W. Taki, D.C. Henshall, Unilateral hippocampal CA3-predominant damage and short latency epileptogenesis after intra-amygdala microinjection of kainic acid in mice. Brain Res. 1213, 140–151 (2008)

    Article  Google Scholar 

  14. E.M. Jimenez-Mateos, T. Engel, P. Merino-Serrais, R.C. McKiernan, K. Tanaka, G. Mouri, T. Sano, C. O’Tuathaigh, J. Waddington, S. Prenter, N. Delanty, M.A. Farrell, D.F. O’Brien, M.R. Conroy, R.L. Stallings, J. deFelipe, D.C. Henshall, Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat. Med. 18(7), 1087–1094 (2012)

    Article  Google Scholar 

  15. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates (Academic Press, New York, 2005)

    Google Scholar 

  16. K.B.J. Franklin, G. Paxinos, The Mouse Brain in Stereotaxic Coordinates (Academic Press, San Diego, 2008)

    Google Scholar 

  17. F. Frigerio, A. Frasca, I. Weissberg, S. Parrella, A. Friedman, A. Vezzani, F.M. Noe, Long-lasting pro-ictogenic effects induced in vivo by rat brain exposure to serum albumin in the absence of concomitant pathology. Epilepsia 53(11), 1887–1897 (2012)

    Article  Google Scholar 

  18. L. Chauvière, N. Rafrafi, C. Thinus-Blanc, F. Bartolomei, M. Esclapez, C. Bernard, Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J. Neurosci. 29(17), 5402–5410 (2009)

    Article  Google Scholar 

  19. J. Seo, S. Jung, S.Y. Lee, H. Yang, B.S. Kim, J. Choi, M. Bang, H.S. Shin, D. Jeon, Early deficits in social behavior and cortical rhythms in pilocarpine-induced mouse model of temporal lobe epilepsy. Exp. Neurol. 241, 38–44 (2013)

    Article  Google Scholar 

  20. H. Poincaré, Sur le problème des trois corps et les équations de la dynamique. Acta Math. 13(1), A3–A270 (1890)

    Article  Google Scholar 

  21. J.P. Eckmann, S.O. Kamphorst, D. Ruelle, Recurrence plots of dynamical systems. Europhys. Lett. 4(9), 973 (1987)

    Article  ADS  Google Scholar 

  22. N. Marwan, Encounters with neighbours: current developments of concepts based on recurrence plots and their applications. Ph.D. Thesis, University of Potsdam (2003)

    Google Scholar 

  23. N. Marwan, M. Carmen Romano, M. Thiel, J. Kurths, Recurrence plots for the analysis of complex systems. Phys. Rep. 438(5), 237–329 (2007)

    Article  ADS  MathSciNet  Google Scholar 

  24. F. Takens, Detecting strange attractors in turbulence, in Dynamical Systems and Turbulence, Warwick 1980 (Springer, Berlin, 1981), pp. 366–381

    Google Scholar 

  25. C.L. Webber, J.P. Zbilut, Recurrence quantification analysis of nonlinear dynamical systems. in Tutorials in Contemporary Nonlinear Methods for the Behavioral Sciences, ed. by M.A. Riley, G.C. Van Orden, pp. 26–94 (2005). http://www.nsf.gov/sbe/bcs/pac/nmbs/chap2.pdf

  26. J. Theiler, S. Eubank, A. Longtin, B. Galdrikian, Farmer J. Doyne, Testing for nonlinearity in time series: the method of surrogate data. Physica D 58(1), 77–94 (1992)

    Article  ADS  MATH  Google Scholar 

  27. J. Gao, Z. Zheng, Direct dynamical test for deterministic chaos and optimal embedding of a chaotic time series. Phys. Rev. E 49(5), 3807 (1994)

    Article  ADS  Google Scholar 

  28. M. Thiel, M.C. Romano, J. Kurths, R. Meucci, E. Allaria, F.T. Arecchi, Influence of observational noise on the recurrence quantification analysis. Physica D 171(3), 138–152 (2002)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  29. T. Schreiber, A. Schmitz, Surrogate time series. Physica D 142(3), 346–382 (2000)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  30. G. Ouyang, X. Li, C. Dang, D.A. Richards, Using recurrence plot for determinism analysis of EEG recordings in genetic absence epilepsy rats. Clin. Neurophysiol. 119(8), 1747–1755 (2008)

    Article  Google Scholar 

  31. T. Schreiber, A. Schmitz, Improved surrogate data for nonlinearity tests. Phys. Rev. Lett. 77(4), 635 (1996)

    Article  ADS  Google Scholar 

  32. R. Barbera, G. La Rocca, M. Rizzi, Grid computing technology and the recurrence quantification analysis to predict seizure occurrence in patients affected by drug-resistant epilepsy, in Data Driven e-Science (Springer, New York, 2011), pp. 493–506

    Google Scholar 

  33. C.L. Webber, Introduction to recurrence quantification analysis RQA version 13.1 README. PDF. http://homepages.luc.edu/~cwebber/RQA131.EXE

  34. R. Hegger, H. Kantz, T. Schreiber, Practical implementation of nonlinear time series methods: the TISEAN package. Chaos 9(2), 413–435 (1999)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  35. K. Klimaszewska, J.J. Żebrowski, Detection of the type of intermittency using characteristic patterns in recurrence plots. Phys. Rev. E 80(2), 026214 (2009)

    Article  ADS  Google Scholar 

  36. J.L. Velazquez, H. Khosravani, A. Lozano, B. Bardakjian, P.L. Carlen, R. Wennberg, Type III intermittency in human partial epilepsy. Eur. J. Neurosci. 11(7), 2571–2576 (1999)

    Article  Google Scholar 

  37. J.L.P. Velazquez, M.A. Cortez, O.C. Snead, R. Wennberg, Dynamical regimes underlying epileptiform events: role of instabilities and bifurcations in brain activity. Physica D 186(3), 205–220 (2003)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  38. J.A. Gorter, P.M.G. Pereira, E.A. Van Vliet, E. Aronica, F.H.L. Da Silva, P.J. Lucassen, Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures. Epilepsia 44(5), 647–658 (2003)

    Article  Google Scholar 

  39. T. Araki, R.P. Simon, W. Taki, J.Q. Lan, D.C. Henshall, Characterization of neuronal death induced by focally evoked limbic seizures in the C57BL/6 mouse. J. Neurosci. Res. 69(5), 614–621 (2002)

    Article  Google Scholar 

  40. A. Vezzani, M. Conti, A. De Luigi, T. Ravizza, D. Moneta, F. Marchesi, M.G. De Simoni, Interleukin-1β immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainic-acid application: functional evidence for enhancement of electrographic seizures. J. Neurosci. 19(12), 5054–5065 (1999)

    Google Scholar 

  41. M. Stead, M. Bower, B.H. Brinkmann, K. Lee, W.R. Marsh, F.B. Meyer, B. Litt, J. Van Gompel, G.A. Worrell, Microseizures and the spatiotemporal scales of human partial epilepsy. Brain 133, 2789–2797 (2010)

    Article  Google Scholar 

  42. A. Bragin, C.L. Wilson, J. Engel, Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41(s6), S144–S152 (2000)

    Article  Google Scholar 

Download references

Acknowledgments

We wish to thank Prof. Charles Webber, who generously provided the source codes of RQA applications used in this work. We also wish to thank Dr. Giuseppe La Rocca (Italian National Institute of Nuclear Physics, Division of Catania, Italy) and Prof. Giuseppe Barbera (Italian National Institute of Nuclear Physics, Division of Catania and Department of Physics and Astronomy of the University of Catania, Italy) for their technical assistance on the usage of Grid Computing resources and services provided by the Italian Grid Infrastructure (IGI, http://www.italiangrid.it/).

Conflict of Interest

Authors have no conflict of interest to declare.

Author information

Authors and Affiliations

  1. Department of Neuroscience, IRCCS—Istituto di Ricerche Farmacologiche Mario Negri, Via La Masa 19, 20156, Milan, Italy

    Massimo Rizzi, Federica Frigerio & Valentina Iori

Authors
  1. Massimo Rizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Federica Frigerio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valentina Iori
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Massimo Rizzi .

Editor information

Editors and Affiliations

  1. Dept. of Cell and Molecular Physiology, Loyola University Chicago, Maywood, Illinois, USA

    Charles L. Webber, Jr.

  2. GIPSA-Lab, University Grenoble Alpes, Grenoble, France

    Cornel Ioana

  3. Potsdam Ins. for Climate Impact Research, Potsdam, Germany

    Norbert Marwan

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this paper

Cite this paper

Rizzi, M., Frigerio, F., Iori, V. (2016). The Early Phases of Epileptogenesis Induced by Status Epilepticus Are Characterized by Persistent Dynamical Regime of Intermittency Type. In: Webber, Jr., C., Ioana, C., Marwan, N. (eds) Recurrence Plots and Their Quantifications: Expanding Horizons. Springer Proceedings in Physics, vol 180. Springer, Cham. https://doi.org/10.1007/978-3-319-29922-8_10

Download citation

Publish with us

Policies and ethics

Search

Navigation