Summary
Purpose: An understanding of the principles governing the behavior of complex neuronal networks, in particular their capability of generating epileptic seizures implies the characterization of the conditions under which a transition from the interictal to the ictal state takes place. Signal analysis methods derived from the theory of nonlinear dynamics provide new tools to characterize the behavior of such networks, and are particularly relevant for the analysis of epileptiform activity.Methods: We calculated the correlation dimension, tested for irreversibility, and made recurrence plots of EEG signals recorded intracranially both during interictal and ictal states in temporal lobe epilepsy patients who were surgical candidates.Results: Epileptic seizure activity often, but not always, emerges as a low-dimensional oscillation. In general, the seizure behaves as a nonstationary phenomenon during which both phases of low and high complexity may occur. Nevertheless a low dimension may be found mainly in the zone of ictal onset and nearby structures. Both the zone of ictal onset and the pattern of propagation of seizure activity in the brain could be identified using this type of analysis. Furthermore, the results obtained were in close agreement with visual inspection of the EEG records.Conclusions: Application of these mathematical tools provides novel insights into the spatio-temporal dynamics of “epileptic brain states”. In this way it may be of practical use in the localization of an epileptogenic region in the brain, and thus be of assistance in the presurgical evaluation of patients with localization-related epilepsy.
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Abbreviations
- ADC:
-
analog to digital converter
- CPS:
-
complex partial seizure
- ECoG:
-
electro corticogram
- EEG:
-
electroencephalogram
- FIR:
-
finite impulse response (filter)
- LGRP:
-
linear Gaussian random process
- log:
-
logarithm with base 10
- MTLE:
-
mesial temporal lobe epilepsy
- PCM:
-
pulse code modulation
- SCECoG:
-
subchonic electro corticogram
- SEEG:
-
stereoelectroencephalogram
- TLE:
-
temporal lobe epilepsy
- QEEG:
-
quantitative EEG (analysis)
- ATL, ATR:
-
anterior temporal left,-right
- MTL, MTR:
-
mid temporal left,-right
- PTL, PTR:
-
posterior temporal left,-right
- AML, AMR:
-
amygdala left,-right
- HCL, HCR:
-
hippocampus left,-right
- G1:
-
input amplifiers common reference electrode
- G2:
-
current-source electrode for compensating potential changes of G1
- i:
-
interictal
- P:
-
pre-ictal
- S:
-
seizure
- C(r,m) :
-
correlation integral
- D2 :
-
correlation dimension
- h :
-
Heaviside or step function
- d :
-
distance between two vectors (maximum norm)
- k :
-
largest delay
- K 2 :
-
correlation entropy
- log:
-
logarithm with base 10
- m :
-
embedding dimension
- N :
-
number of (reconstructed) vectors in phase space
- ν :
-
sampling frequency
- T :
-
time-window for the ‘Theiler correction’
- r :
-
radius of a sphere in phase space
- \(\vec V_m (i)\) :
-
(reconstructed) vector in m-dimensional phase space
- W,T :
-
number of samples and time span of the window for the “Theiler correction”
- x i :
-
samplei of the time series
- t :
-
time
- x,\(\dot x, \ddot x\) :
-
position, velocity and acceleration of the beam
- δ:
-
friction coefficient
- γ:
-
amplitude of the driving force
- ω:
-
angular frequency of the driving force
References
Achermann, P., Hartmann, R., Gunzinger, A., Guggenbuhl, W. and Borbély, A.A. All-night sleep EEG and artificial stochastic control signals have similar correlation dimensions. Electroenceph. clin. Neurophysiol., 1994, 90: 384–387.
Albano, A.M., Muench, J., Schwartz, C, Mees, A.I., and Rapp, P.E. Singular-value decomposition and the Grassberger-Procaccia algorithm. Phys. Rev. A 1988, 38, 3017–3026.
Babloyantz, A. and Destexhe, A. Low dimensional chaos in an instance of epilepsy. Proc. Nat. Acad. Sci. (USA), 1986, a3: 3513–3517.
Blinowska, K.J. and Malinowski, M. Non-linear and linear forecasting of the EEG time series. Biol. Cybern., 1991, 66: 159–165.
Brekelmans, G.J.F., van Emde Boas, W., Velis, D.N., van Huffelen, A.C., Debets, R.M.Chr. and van Veelen, C.W.M. Mesial temporal versus neocortical temporal lobe seizures: demonstration of different electroencephalographic spreading patterns by combined use of subdural and intracerebral electrodes. J. Epilepsy, 1995, 8: 308–320.
Cerf, R., Ouldénoune, M., Ben Maati, M.L., El Ousdad, E.H.and Daoudi, A. Wave-separation in complex systems. Application to brain-signals. J. of Biol. Phys., 1994, 19: 223–233.
Delmas, A. and Pertuiset, B. Cranio-cerebral topometry in man. Paris, Masson, and Oxford, Blackwell Scientific Publications. 1959.
Diks, C, van Houwelingen, J.C., Takens, F. and DeGoede, J. Reversibility as a criterion for discriminating time series. Phys. Lett. A, 1995, 201: 221–228.
Eckmann, J.P., Oliffson Kamphorst, S. and Ruelle, D. Recurrence plots of dynamical systems. Europhys. Lett., 1987, 4(9): 973–977.
Elbert, T., Ray, W.J., Kowalik, Z.J., Skinner, J.E., Graf, K.E. and Birbaumer, N. Chaos and physiology: deterministic chaos in excitable cell assemblies. Physiol Rev, 1994, 74(1): 1–47.
Frank, G.W., Lookman, T., Nerengerg, M.A.H., Essex, C., Lemieux, J. and Blume, W. Chaotic time series analyses of epileptic seizures. Physica D, 1990, 46: 427–438.
Fraser, A.M. and Swinney, H.L. Independent coordinates for strange attractors from mutual information. Phys. Rev., 1986, 33A: 1134–1140.
Freeman, W.J.. Societies of Brains: A Study in the Neuroscience of Love and Hate. Lawr. Erlb. Assoc.Publ., Hillsdale, New Jersey, 1995.
Gotman, J. Automatic recognition of epileptic seizures in the EEG. Electroenceph. clin. Neurophysiol., 1982, 54: 530–540.
Gotman, J. Automatic seizures detection: improvements and evaluation. Electroenceph. clin. Neurophysiol., 1990, 54: 530–540.
Grassberger, P. and Procaccia, I. Measuring the strangeness of strange attractors. Physica D, 1983, 9: 189–208.
Grassberger, P., Hegger, R., Kantz, H., Schaffrath, C. and Schreiber, Th. On noise reduction methods for chaotic data. Chaos, 1993, 3: 127–141.
Guckenheimer, J. and Holmes, P. Nonlinear oscillations, dynamical systems and bifurcations of vector fields. Springer, Heidelberg, 1983.
Hammel, S.M. A noise reduction method for chaotic systems. Phys. Lett., A., 1990, 160: 421–428.
Havstad, J.W. and Ehlers, C.L. Attractor dimension of nonstationary dynamical systems from small data sets. Physical Review A, 1989, 39: 845–853.
Hayashi, H. and Ishizuka, S. Chaotic responses of the hippocampal CA3 region to a mossy fiber stimulation in vitro. Brain Res., 1995, 686(2): 194–206.
Hernández, J.L., Valdés, J.L., Biscay, R., Jiménez, J.C. and Valdés, P. EEG predictability: properness of non-linear forecasting methods. Int. J. Bio-Med. Comp., 1995, 38: 197–206.
van der Heyden, M.J., Diks, C, Pijn, J.P.M. and Velis, D.N. Time reversibility of intracranial human EEG recordings in temporal lobe epilepsy. Phys.Lett.A, 1996, 216: 283–288.
Iasemidis, L.D., Sackellares, J.C, Zaveri, H.P. and Williams, W.J. Phase space topography and the Lyapunov exponent of electrocorticograms in partial seizures. Brain Topogr., 1990, 2: 187–201.
Iasemidis, L.D., Barreto, A., Uthman, B.M., Roper, S., Sackellares, I.C.. Spatio temporal evolution of dynamical measures precedes onset of mesial temporal lobe seizures. Epilepsia, 1994, 35 (Suppl. 8): 133.
Iasemidis, L.D., Principe, J.C, Czaplewski, J.M., Gilmore, R.L., Roper, S.N. and Sackellares, I.C. Spatiotemporal transition to epileptic seizures: a nonlinear dynamical analysis of scalp and intracranial EEG recordings. In: F.L. Silva, J.C. Principe and L.B. Almeida (Ed.), Spatiotemporal Models in Biological and Artificial Systems. IOS Press, Amsterdam, 1996: 81–88.
Ishizuka, S. and Hayashi, H. Chaotic and phase-locked responses of the somatosensory cortex to a periodic medial lemniscus stimulation in the anesthetized rat. Brain Res., 1996, 723: 46–60.
Kaboudan MA, 1993. A complexity test based on the correlation integral. Phys. Lett. A 181: 381–386.
Kantz H and Schreiber T. Dimension estimates and physiological data. Chaos, 1995, 5 (1): 143–154.
Kaplan, D.T. and Glass, L. Direct test for deterministism in a time series. Phys. Rev. letters, 1992, 68: 427–430.
Lehnertz, K and Elger, C.E. Spatio-temporal dynamics of the primary epileptogenic area in temporal lobe epilepsy characterized by neuronal complexity loss. Electroenceph. clin. Neurophysiol., 1995, 95: 108–117.
Lieb, J.P., Dasheiff, R.M. and Engel Jr, J. Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia, 1991, 32(6): 822–837.
Lopes da Silva, F.H., Witter, M.P., Boeijinga, P.H. and Lohman, A.H.M. Anatomic organization and physiology of the limbic cortex. Phys. Rev., 1990, 70(2): 453–511.
Lopes da Silva, F.H. and Pijn, J.P.M. Epilepsy: network models of generation. In: M. A. Arbib (Ed.), The Handbook of Brain Theory and Neural Networks. The MIT Press, Massachusetts, USA, 1995: 367–369
Lopes da Silva F. H., Pijn J.P.M.and Velis D.N. Signal processing of EEG: evidence for chaos or noise. An application to seizure activity in epilepsy. In: Advances in Processing and Pattern Analysis of Biological Signals. Edited by I. Gath and G.F. Inbar. Plenum Press, New York, 1996.
Lopes da Silva, F.H., Pijn, J.P.M., Velis, D. and Nijssen, P.C.G. Alpha rhythms: noise, dynamics and models. In: E. Basar, R. Hari, F.H. Lopes da Silva and M. Schürmann (Ed.), Alpha Activity: Cognitive and Sensory Behaviour, Boston, In Press.
Muhlnickel, W., Rendtorff, N., Kowalik, J., Rockstroh, B., Miltner, W. and, Elbert, T. Testing the determinism of EEG and MEG. Integrative Physiological and Behavioral Science, 1994, 29: 262–269.
Müller-Gerking, J., Martinerie, J., Neuenschwander, S., Pezard, L., Renault, B. and Varela, F.J. Detecting non-linearities in neuro-electrical signals: a study of synchronous local field potentials. Physica D, 1996, 94: 65–91.
van Neerven, J.M.A.M. Determination of the correlation dimension from a time series, applications to rat EEGs: sleep, theta rhythm and epilepsy. Master's thesis. Dept. Exp. Zoology, University of Amsterdam, 1987.
Osborne, A.R., Kirwan Jr, A.D., Provenzale, A. and Bergamasco, L. A Search for chaotic behavior and mesoscale motions in the pacific ocean. Physica D, 1986, 23: 75–83.
Osborne, A.R. and Provenzale, A. Finite correlation dimension for stochastic systems with power-law spectra. Physica D, 1989, 35: 357–381.
Palus, M. Testing for Nonlinearity in the EEG. Technical report CCSR-92-16, Center for Complex Systems Research, University of Illinois at Urbana-Champaign, 1992.
Pezard, L., Martinerie, J., Müller-Gerking, J., Varela, F.J. and Renault, B. Entropy quantification of human brain spatiotemporal dynamics. Physica D, 1996, 96: 344–354.
Pijn, J.P.M. Quantitative evaluation of EEG signals in epilepsy; nonlinear associations, time delays and nonlinear dynamics. Ph.D. thesis, Rodopi, Amsterdam, 1990.
Pijn, J.P.M., van Neerven, J., Noest, A., Lopes da Silva, F.H. Chaos or noise in EEG signals: dependence on state and brain site. Electroenceph. clin. Neurophysiol., 1991, 79: 371–381.
Pijn, J.P.M., Velis, D.N., van Emde Boas, W. and Lopes da Silva, F.H. Determination of seizure onsetby means of chaos theory analysis of EEG records. Epilepsia, suppl., 1992, 33: 64.
Pradhan, N. and Narayana Dutt, D. A nonlinear perspective in understanding the neurodynamics of EEG. Comput. Biol. Med., 1993, 23: 425–442.
Prichard, D. and Theiler, J. Generating surrogate data for time series with several simultaneously measured variables. Phys. Rev. Lett., 1994, 73: 951–954.
Pritchard, W.S. and Duke, D.W. Measuring chaos in the brain: a tutorial review of nonlinear dynamical EEG analysis. Int. J. Neurosci., 1992, 67: (1–4): 31–80.
Provenzale, A., Smith, L.A., Vio, R. and Murate, G. Distinguishing between low-dimensional dynamics and randomness in measured time series. Physica D, 1992, 58: 31–49.
Rapp, P.E. A guide to dynamical analysis. Integr. Phys. and Behav. Sc., 1994, 29: 311–327.
Rapp, P.E., Albano, A.M., Schmah, A.M. and Farwell, L.A. Filtered noise can mimic low-dimensional chaotic attractors. Phys. Rev. E, 1993, 47: 2289–2297.
Rapp, P.E., Albano, A.M., Zimmerman, I.D. and Jimenéz-Montano, M.A. Phase-randomized surrogates can produce spurious identifications of non-random structure. Phys. Lett. A, 1994, 192: 27–33.
Rombouts, S.A.R.B., Keunen, R.W.M. and Stam, C.J. Investigation of nonlinear structure in multichannel EEG. Phys. Lett. A, 1995, 202: 352–358.
Schiff, S.J. and Chang, T. Differentiation of linearly correlated noise from chaos in a biologic system using surrogate data. Biol. Cybern., 1992, 67: 387–393.
Skarda, C.A. and Freeman, W.J. How brains make chaos in order to make sense of the world. Behav. Brain Sci., 1987, 10: 161–195.
Soong, A.C.K. and Stuart, C.I.J.M. Evidence of chaotic dynamics underlying the human alpha-rhythm electroencephalogram. Biol Cybern., 1989, 62: 55–62.
Takens, F. Detecting strange attractors in turbulence. In: Dynamical Systems and Turbulence, Warwick 1980. Lecture Notes in Mathematics, 1981, 898: 366–381.
Takens, F. Detecting nonlinearities in stationary time series. Int. J. Bifurc. Chaos, 1993, 3(2): 241–256.
Theiler, J. Spurious dimension from correlation algorithms applied to limited time-series data. Phys. Rev. A, 1986, 34: 2427–2432.
Theiler, J. On the evidence for low-dimensional chaos in an epileptic electroencephalogram. Physics Letters A, 1995, 196: 335–341.
Theiler, J., Eubank, S., Longtin, A., Galdrikian, B. and Doyne Farmer, J. Testing for nonlinearity in time series: the method of surrogate data. Physica D, 1992A, 58: 77–94.
Theiler, J., Galdrikian, B., Longtin, A., Eubank, S. and Farmer, J.D. In: M. Casdagli and S. Eubank (Ed.), Nonlinear Modeling and Forecasting. Addison-Wesley, Reading, MA., 1992B.
Theiler, J. and Rapp, P.E. Re-examination of the evidence for low-dimensional nonlinear structure in the human electroencephalogram. Electroenceph. clin. Neurophysiol., 1996, 98: 213–223.
Townsend III, J. B. and J. Engel Jr, J. “Clinicopathological correlations of low voltage fast and high amplitude spike and wave mesial temporal stereoencephalographic ictal onsets.” Epilepsia, 1991, 32(3): 21.
van Veelen, C.W.M., Debets, R.M.Chr., Van Huffelen, A.C., Van Emde Boas, W., Binnie, C.D., Storm van Leeuwen, W., Velis, D.N., van Dieren, A. Combined use of subdural and intracerebral electrodes in preoperative evaluation of epilepsy. Neurosurgery, 1990, 26: 93–101.
Wadman, W.J., Juta, A.J.A., Kamphuis, W. and Somjen, G.G. Current source density of sustained potential shifts associated with electrographic seizures and with spreading depression in rat hippocampus. Brain Research, 1992, 570: 85–91.
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We thank Tjeerd olde Scheper for his help in doing the analyses and Wouter Blanes for his continuous support in producing code for our computer as well as text for this manuscript. This work was subsidized in part by CLEO (Dutch Commission for research in Epilepsy), grants A71 and A88, by the NEF (Dutch Epilepsy Foundation), grant 95-01 and by NWO (Netherlands Organization for Scientific Research), grant 629-61-270.
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Pijn, J.P.M., Velis, D.N., van der Heyden, M.J. et al. Nonlinear dynamics of epileptic seizures on basis of intracranial EEG recordings. Brain Topogr 9, 249–270 (1997). https://doi.org/10.1007/BF01464480
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DOI: https://doi.org/10.1007/BF01464480