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Seizure Predictability in an Experimental Model of Epilepsy

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Data Mining in Biomedicine

Abstract

We have previously reported preictal spatiotemporal transitions in human mesial temporal lobe epilepsy (MTLE) using short term Lyapunov exponent (STL max ) and average angular frequency (\( \Omega \) ). These results have prompted us to apply the quantitative nonlinear methods to a limbic epilepsy rat (CLE), as this model has several important features of human MTLE. The present study tests the hypothesis that preictal dynamical changes similar to those seen in human MTLE exist in the CLE model. Forty-two, 2-hr epoch data sets from 4 CLE rats (mean seizure duration 74±20 sec) are analyzed, each containing a focal onset seizure and intracranial data beginning 1 hr before the seizure onset. Three nonlinear measures, correlation integral, short-term largest Lyapunov exponent and average angular frequency are used in the current study. Data analyses show multiple transient drops in STL max values during the preictal period followed by a significant drop during the ictal period. Average angular frequency values demonstrate transient peaks during the preictal period followed by a significant peak during the ictal period. Convergence among electrode sites is also observed in both STL max and \( \Omega \) values before seizure onset. Results suggest that dynamical changes precede and accompany seizures in rat CLE. Thus, it may be possible to use the rat CLE model as a tool to refine and test real-time seizure prediction, and closed-loop intervention techniques.

This study was supported by NIH grant RO1EB002089, Children’s Miracle Network, University of Florida Division of Sponsored Research, and Department of Veterans Affairs.

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References

  1. R. Agarwal and J. Gotman. Adaptive segmentation of electroencephalographic data using a nonlinear energy operator. Proceedings of the 1999 IEEE International Symposium on Circuits and Systems, Orlando, FL, 1999.

    Google Scholar 

  2. T. Babb and I. Najm. Hippocampal Sclerosis: Pathology, Electrophysiology, and Mechanisms of Epileptogenesis. In E. Wyllie, editor, The Treatment of Epilepsy: Principles and Practice, pages 105–114. Williams and Wilkins, 2001.

    Google Scholar 

  3. S.M. Bawin, A.R. Sheppard, M.D. Mahoney, M. Abu-Assal, and W.R. Adey. Comparison between the effects of extra cellular direct and sinusoidal currents on excitability in hippocampal slices. Brain Research, 362: 350–354, 1986.

    Article  PubMed  CAS  Google Scholar 

  4. E.H. Bertram, E.W. Lothman, and N.J. Lenn. The hippocampus in experimental chronic epilepsy: a morphometric analysis. Annals of Neurology, 27: 43–48, 1990.

    Article  PubMed  CAS  Google Scholar 

  5. E.H. Bertram and J. Cornett. The ontogeny of seizures in a rat model of limbic epilepsy: evidence for a kindling process in the development of chronic spontaneous seizures. Brain Research, 625: 295–300, 1993.

    Article  PubMed  CAS  Google Scholar 

  6. E.H. Bertram and J. Cornett. The evolution of a rat model of chronic spontaneous limbic seizures. Brain Research, 661: 157–162, 1994.

    Article  PubMed  CAS  Google Scholar 

  7. E.H. Bertram. Functional anatomy of spontaneous seizures in a rat model of limbic epilepsy. Epilepsia, 38: 95–105, 1997.

    Article  PubMed  CAS  Google Scholar 

  8. E.H. Bertram, J.M. Williamson, J.F. Cornett, S. Spradlin, and Z.F. Chen. Design and construction of a long term continuous video-EEG monitoring unit for simultaneous recording of multiple small animals. Brain Research Protocols, 2: 85–97, 1997.

    Article  PubMed  CAS  Google Scholar 

  9. M. Bikson, J. Lian, P.J. Hahn, W.C. Stacey, C. Sciortino, and D.M. Durand. Suppression of epileptiform activity by high frequency sinusoidal fields in rat hippocampal slices. The Journal of Physiology, 531: 181–191, 2001.

    Article  PubMed  CAS  Google Scholar 

  10. T.R. Browne and G.L. Holmes. Epilepsy. New England Journal of Medicine, 344: 1145–1151, 2001.

    Article  PubMed  CAS  Google Scholar 

  11. P.R. Carney, D.S. Shiau, P.M. Pardalos, L.D. Iasemidis, W. Chaovalitwongse, and J.C. Sackellares. Nonlinear neurodynamical features in an animal model of generalized epilepsy. In P.M. Pardalos, J.C. Sackellares, P.R. Carney, and L.D. Iasemidis, editors, Quantitative Neuroscience, pages 37–51. Kluwer Academic Publishers, Boston, 2004.

    Google Scholar 

  12. P.R. Carney, S.P. Nair, L.D. Iasemidis, D.S. Shiau, P.M. Pardalos, D. Shenk, W. Norman, and J.C. Sackellares. Quantitative analysis of EEG in the rat limbic epilepsy model. Neurology, 62(7, Suppl. 5): A282–A283, 2004.

    Google Scholar 

  13. M.C. Casdagli, L.D. Iasemidis, J.C. Sackellares, S.N. Roper, R.L. Gilmore, R.S. Savit. Characterizing nonlinearity in invasive EEG recordings from temporal lobe epilepsy. Physica D, 99: 381–399, 1996.

    Article  Google Scholar 

  14. M.C. Casdagli, L.D. Iasemidis, R.S. Savit, R.L. Gilmore, S.N. Roper, and J.C. Sackellares. Non-linearity in invasive EEG recordings from patients with temporal lobe epilepsy. Electroencephalography and Clinical Neurophysiology, 102: 98–105, 1997.

    Article  PubMed  CAS  Google Scholar 

  15. M. D’Alessandro, R. Esteller, G. Vachtsevanos, A. Hinson, J. Echauz, and B. Litt. Epileptic seizure prediction using hybrid feature selection over multiple intracranial EEG electrode contacts: a report of four patients. IEEE Transactions on Biomedical Engineering, 50(5): 603–615, 2003.

    Article  PubMed  Google Scholar 

  16. H. Degn, A.V. Holden, and L.F. Olsen. Chaos in Biological Systems. Kluwer Academic/Plenum Publishers, 1986.

    Google Scholar 

  17. M.J. Denslow, T. Eid, F. Du, R. Schwarcz, E.W. Lothman, and O. Steward. Disruption of inhibition in area CA1 of the hippocampus in a rat model of temporal lobe epilepsy. Journal of Neurophysiology, 86(5): 2231–2245, 2001.

    PubMed  CAS  Google Scholar 

  18. D.M. Durand. Electric field effects in hyperexcitable neural tissue: A review. Radiation Protection Dosimetry, 106: 325–331, 2003.

    PubMed  CAS  Google Scholar 

  19. H.G. Eder, D.B. Jones, R.S. Fisher. Local perfusion of diazepam attenuates interictal and ictal events in the bicuculline model of epilepsy in rats. Epilepsia, 38: 516–521, 1997.

    Article  PubMed  CAS  Google Scholar 

  20. H.G. Eder, A. Stein, and R.S. Fisher. Interictal and ictal activity in the rat cobalt/pilocarpine model of epilepsy decreased by local perfusion of diazepam. Epilepsy Research, 29: 17–24, 1997.

    Article  PubMed  CAS  Google Scholar 

  21. E.E. Fanselow, A.P. Reid, and M.A. Nicolelis. Reduction of pentylenetetrazole-induced seizure activity in awake rats by seizure-triggered trigeminal nerve stimulation. Journal of Neuroscience, 20: 8160–8168, 2000.

    PubMed  CAS  Google Scholar 

  22. N.B. Fountain, J. Bear, E.H. Bertram, and E.W. Lothman. Responses of deep entorhinal cortex are epileptiform in an electrogenic rat model of chronic temporal lobe epilepsy. Journal of Neurophysiology, 80: 230–240, 1998.

    PubMed  CAS  Google Scholar 

  23. L. Glass, A.L. Goldberger, M. Courtemanche, and A. Shrier. Nonlinear dynamics, chaos and complex cardiac arrhythmias. Proceedings of the Royal Society of London, Series A, Mathematical and Physical Sciences, A413, pp. 9–26, 1987.

    Article  Google Scholar 

  24. P. Gloor. Neurobiological substrates of ictal behavioral changes. Advances in Neurology, 55: 1–34, 1991.

    PubMed  CAS  Google Scholar 

  25. P. Grassberger and I. Procaccia. Measuring the strangeness of strange attractors. Physica D, 9: 189–208, 1983.

    Article  Google Scholar 

  26. P. Grassberger. An optimal box-assisted algorithm for fractal dimensions. Physics Letters A, 148: 63–68, 1990.

    Article  Google Scholar 

  27. M. Gruenthal. Electroencephalographic and histological characteristics of a model of limbic status epilepticus permitting direct control over seizure duration. Epilepsy Research, 29: 221–232, 1998.

    Article  PubMed  CAS  Google Scholar 

  28. W.A. Hauser. Incidence and prevalence. In J. Engel Jr. and T.A. Pedley, editors, Epilepsy: A Comprehensive Textbook, pages 47–57. Lippincott-Raven, Philadelphia, 1997.

    Google Scholar 

  29. L.D. Iasemidis, J.C. Sackellares, H.P. Zaveri, and W.J. Williams. Phase space topography of the electrocorticogram and the Lyapunov exponent in partial seizures. Brain Topography, 2: 187–201, 1990.

    Article  PubMed  CAS  Google Scholar 

  30. L.D. Iasemidis and J.C. Sackellares. The temporal evolution of the largest Lyapunov exponent on the human epileptic cortex. In D.W. Duke and W.S. Pritchard, editors, Measuring Chaos in the Human Brain, pages 49–82. World Scientific, Singapore, 1991.

    Google Scholar 

  31. L.D. Iasemidis. On the Dynamics of the Human Brain in Temporal Lobe Epilepsy. PhD Thesis, University of Michigan, Ann Arbor, 1991.

    Google Scholar 

  32. L.D. Iasemidis, L.D. Olson, R.S. Savit, and J.C. Sackellares. Time dependencies in the occurrence of epileptic seizures. Epilepsy Research, 17:81–94, 1994.

    Article  PubMed  CAS  Google Scholar 

  33. L.D. Iasemidis, J.C. Principe, J.M. Czaplewski, et al. Spatiotemporal transition to epileptic seizures: A nonlinear dynamical analysis of scalp and intracranial EEG recordings. In F.H. Lopes de Silva, J.C. Principe, and L.B. Almeida, editors, Spatiotemporal Models in Biological and Artificial Systems, pages 81–88. IOS Press, Amsterdam, 1997.

    Google Scholar 

  34. L.D. Iasemidis, J.C. Principe, J.C. Sackellares. Measurement and quantification of spatiotemporal dynamics of human epilepogenic seizures. In: M. Akay, editor, Nonlinear Signal Processing in Medicine. IEEE Press, 1999.

    Google Scholar 

  35. L.D. Iasemidis, P.M. Pardalos, J.C. Sackellares, and D.S. Shiau. Quadratic binary programming and dynamical system approach to determine the predictability of epileptic seizures. Journal of Combinatorial Optimization, 5: 9–26, 2001.

    Article  Google Scholar 

  36. L.D. Iasemidis, D.S. Shiau, W. Chaowolitwongse, J.C. Sackellares, P.M. Pardalos, J.C. Principe, P.R. Carney, A. Prasad, B. Veeramani, and K. Tsakalis. Adaptive epileptic seizure prediction system. IEEE Transactions on Biomedical Engineering, 50(5): 616–627, 2003.

    Article  PubMed  Google Scholar 

  37. L.D. Iasemidis, P.M. Pardalos, D.S. Shiau, W. Chaovalitwongse, M. Narayanan, S. Kumar, P.R. Carney, and J.C. Sackellares. Prediction of human epileptic seizures based on optimization and phase changes of brain electrical activity. Optimization Methods and Software, 18: 81–104, 2003.

    Article  Google Scholar 

  38. B.H. Jansen. Is it and so what? A critical review of EEG-chaos. In D.W. Duke and W.S. Pritchard, editors, Measuring Chaos in the Human Brain. World Scientific, Singapore, 1991.

    Google Scholar 

  39. K.Y. Jung, J.M. Kim, and D.W. Kim. Nonlinear dynamic characteristics of electroencephalography in a high-dose pilocarpine-induced status epilepticus model. Epilepsy Research, 54: 179–188, 2003.

    Article  PubMed  Google Scholar 

  40. J.F. Kaiser. On a simple algorithm to calculate the “energy” of a signal. ICASSP, 381–384, 1990.

    Google Scholar 

  41. J.A.S. Kelso, A.J. Mandell, M.F. Shlesinger. Dynamic patterns in complex systems. World Scientific, Singapore, 1988.

    Google Scholar 

  42. M. Le Van Quyen, J. Martinerie, V. Navarro, M. Baulac, and F.J. Varela. Characterizing neurodynamic changes before seizures. Journal of Clinical Neurophysiology, 18: 191–208, 2001.

    Article  Google Scholar 

  43. M. Le Van Quyen, J. Martinerie, V. Navarro, P. Boon, M. D’Have, C. Adam, B. Renault, F. Varela, and M. Baulac. Anticipation of epileptic seizures from standard EEG recordings. Lancet, 357: 183–188, 2001.

    Article  Google Scholar 

  44. K. Lehnertz and C.E. Elger. Can epileptic seizures be predicted? Evidence from nonlinear time series analysis of brain electrical activity. Physical Review Letters, 80: 5019–5022, 1998.

    Article  CAS  Google Scholar 

  45. K. Lehnertz, R.G. Andrzejak J. Arnhold, T. Kreuz, F. Mormann, C. Rieke, G. Widman, and C.E. Elger. Nonlinear EEG analysis in epilepsy: Its possible use for interictal focus localization, seizure anticipation, and prevention. Journal of Clinical Neurophysiology, 18: 209–222, 2001.

    Article  PubMed  CAS  Google Scholar 

  46. B. Litt, R. Esteller, J. Echauz, M. D’Alessandro, R. Short, T. Henry, P. Pennell, C. Epstein, R. Bakay, M. Dichter, and G. Vachtsevanos. Epileptic seizures may begin hours in advance of clinical onset: a report of five patients. Neuron, 30: 51–64, 2001.

    Article  PubMed  CAS  Google Scholar 

  47. W. Loscher. Animal models of intractable epilepsy. Progress in Neurobiology, 53: 239–258, 1997.

    Article  PubMed  CAS  Google Scholar 

  48. W. Loscher. Animal models of epilepsy for the development of antiepileptogenic and disease-modifying drugs. A comparison of the pharmacology of kindling and post-status epilepticus models of temporal lobe epilepsy. Epilepsy Research, 50: 105–123, 2002.

    Article  PubMed  CAS  Google Scholar 

  49. E.W. Lothman, E.H. Bertram, J. Kapur, and J.L. Stringer. Recurrent spontaneous hippocampal seizures in the rat as a chronic sequela to limbic status epilepticus. Epilepsy Research, 6: 110–118, 1990.

    Article  PubMed  CAS  Google Scholar 

  50. E.W. Lothman, E.H. Bertram, and J.L. Stringer. Functional anatomy of hippocampal seizures. Progress in Neurobiology, 37: 1–82, 1991.

    Article  PubMed  CAS  Google Scholar 

  51. P.S. Mangan and E.W. Lothman. Profound disturbances of pre-and postsynaptic GABA(B)-receptor-mediated processes in region CA1 in a chronic model of temporal lobe epilepsy. Journal of Neurophysiology, 76: 1282–1296, 1996.

    PubMed  CAS  Google Scholar 

  52. R. Manuca and R. Savit. Stationarity and nonstationarity in time series analysis. Physica D, 99: 134–161, 1996.

    Article  Google Scholar 

  53. M. Markus, S.C. Muller, G. Nicolis. From chemical to biological organization. Springer-Verlag, Berlin, New York, 1988.

    Google Scholar 

  54. J. Martinerie, C. Adam, M. Le Van Quyen, M. Baulac, S. Clemenceau, B. Renault, and F.J. Varela. Epileptic seizures can be anticipated by nonlinear analysis. Nature Medicine, 4: 1173–1176, 1998.

    Article  PubMed  CAS  Google Scholar 

  55. R.M. May. Simple mathematical models with very complicated dynamics. Nature, 261: 459–467, 1976.

    Article  PubMed  CAS  Google Scholar 

  56. G. Mayer-Kress. Dimension and entropies in chaotic systems, Springer-Verlag, Berlin, 1986.

    Google Scholar 

  57. S.P. Nair, D.S. Shiau, W.M. Norman, D. Shenk, W. Suharitdamrong, L.D. Iasemidis, P.M. Pardalos, J.C. Sackellares, and P.R. Carney. Dynamical changes in the rat chronic limbic epilepsy model. Epilepsia, 45(S7): 211–212, 2004.

    Google Scholar 

  58. M. Palus. Testing for nonlinearity using redundancies: quantitative and qualitative aspects. Physica D, 80: 186–205, 1995.

    Article  Google Scholar 

  59. M. Palus. Nonlinearity in normal human EEG: cycles, temporal asymmetry, nonstationarity and randomness, not chaos. Biological Cybernetics, 75: 389–396, 1996.

    Article  PubMed  CAS  Google Scholar 

  60. J.P. Pijn, J. Van Neerven, A. Noest, and F.H. Lopes da Silva. Chaos or noise in EEG signals; dependence on state and brain site. Electroencephalography and Clinical Neurophysiology, 79: 371–381, 1991.

    Article  PubMed  CAS  Google Scholar 

  61. M. Quigg, E.H. Bertram, T. Jackson, and E. Laws. Volumetric magnetic resonance imaging evidence of bilateral hippocampal atrophy in mesial temporal lobe epilepsy. Epilepsia, 38: 588–594, 1997.

    Article  PubMed  CAS  Google Scholar 

  62. M. Quigg, M. Staume, M. Menaker, and E.H. Bertram. Temporal distribution of partial seizures: Comparison of an animal model with human partial epilepsy. Annals of Neurology, 43: 748–755, 1998.

    Article  PubMed  CAS  Google Scholar 

  63. R.Q. Quiroga, H. Garcia, and A. Rabinowicz. Frequeny evolution during tonic-clonic seizures. Electromyography and Clinical Neurophysiology, 42: 323–331, 2002.

    PubMed  Google Scholar 

  64. R.J. Racine. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalography and Clinical Neurophysiology, 32: 281–294, 1972.

    Article  PubMed  CAS  Google Scholar 

  65. K.A. Richardson, B.J. Gluckman, S.L. Weinstein, C.E. Glosch, J.B. Moon, R.P. Gwinn, K. Gale, and S.J. Schiff. In vivo modulation of hippocampal epileptiform activity with radial electric fields. Epilepsia 44: 768–777, 2003.

    Article  PubMed  Google Scholar 

  66. J.C. Sackellares, L.D. Iasemidis, H.P. Zaveri, and W.J. Williams. Measurement of chaos to localize seizure onset. Epilepsia, 30(5): 663, 1989.

    Google Scholar 

  67. Y. Salant, I. Gathe, and O. Henriksen. Prediction of epileptic seizures from two-channel EEG. Medical and Biological Engineering and Computing, 36: 549–556, 1998.

    Article  PubMed  CAS  Google Scholar 

  68. J.P. Stables, E.H. Bertram, H.S. White, D.A. Coulter, M.A. Dichter, M.P. Jacobs, W. Loscher, D.H. Lowenstein, S.L. Moshe, J.L. Noebels, and M. Davis. Models for epilepsy and epileptogenesis: Report from the NIH workshop, Bethesda, Maryland. Epilepsia, 43: 1410–1420, 2002.

    Article  PubMed  Google Scholar 

  69. S. Sunderam, I. Osorio, M.G. Frei, and J.F. Watkins. Stochastic modeling and prediction of experimental seizures in Sprague-Dawley rats. Journal of Clinical Neurophysiology, 18: 275–282, 2001.

    Article  PubMed  CAS  Google Scholar 

  70. F. Takens. Detecting strange attractors in turbulence. In D.A. Rand and L.S. Young, editors, Dynamical systems and turbulence: lecture notes in mathematics, pages 366–381. Springer-Verlag, 1981.

    Google Scholar 

  71. J. Theiler. Spurious dimension from correlation algorithms applied to limited time-series data. Physical Review A, 34: 2427–2433, 1986.

    Article  PubMed  Google Scholar 

  72. J. Theiler, B. Galdrikian, S. Eubank, and J.D. Farmer. Using surrogate data to detect non-linearity in time series. In M.C. Casdagli and S. Eubank, editors, Nonlinear Modeling and Forecasting, pages 163–188. Addison-Wesley, Reading, MA, 1991.

    Google Scholar 

  73. L. Vercueil, A. Benazzouz, C. Deransart, K. Bressand, C. Marescaux, A. Depaulis, and A.L. Benabid. High-frequency stimulation of the subthalamic nucleus suppresses absence seizures in the rat: comparison with neurotoxic lesions. Epilepsy Research, 31: 39–46, 1998.

    Article  PubMed  CAS  Google Scholar 

  74. A. Wolf, J.B. Swift, H.L. Swinney, and J.A. Vastanao. Determining Lyapunov exponents from a time series. Physica D, 16: 285–317, 1985.

    Article  Google Scholar 

  75. J. Zabara. Inhibition of experimental seizures in canines by repetitive vagal stimulation. Epilepsia, 33: 1005–1012, 1992.

    Article  PubMed  CAS  Google Scholar 

  76. H. Zaveri, W.J. Williams, and J.C. Sackellares. Energy based detectors of seizures. Presented at 15th Annual International Conference on Engineering and Medicine in Biology, 1993.

    Google Scholar 

  77. H.P. Zaveri, W.J. Williams, J.C. Sackellares, A. Beydoun, R.B. Duck-row, and S.S. Spencer. Measuring the coherence of intracranial electroencephalograms. Clinical Neurophysiology, 110: 1717–1725, 1999.

    Article  PubMed  CAS  Google Scholar 

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Nair, S.P. et al. (2007). Seizure Predictability in an Experimental Model of Epilepsy. In: Pardalos, P.M., Boginski, V.L., Vazacopoulos, A. (eds) Data Mining in Biomedicine. Springer Optimization and Its Applications, vol 7. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-69319-4_27

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