Mapping the epileptic brain with EEG dynamical connectivity: Established methods and novel approaches

  • Margarita Papadopoulou
  • Kristl Vonck
  • Paul Boon
  • Daniele MarinazzoEmail author
Regular Article
Part of the following topical collections:
  1. Focus Point on Advanced Physical Methods in Brain Research


Several algorithms rooted in statistical physics, mathematics and machine learning are used to analyze neuroimaging data from patients suffering from epilepsy, with the main goals of localizing the brain region where the seizure originates from and of detecting upcoming seizure activity in order to trigger therapeutic neurostimulation devices. Some of these methods explore the dynamical connections between brain regions, exploiting the high temporal resolution of the electroencephalographic signals recorded at the scalp or directly from the cortical surface or in deeper brain areas. In this paper we describe this specific class of algorithms and their clinical application, by reviewing the state of the art and reporting their application on EEG data from an epileptic patient.


Granger Causality Seizure Onset Transfer Entropy Scalp Electrode Seizure Detection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    F. Mormann, R.G. Andrzejak, C.E. Elger, K. Lehnertz, Brain 130, 314 (2007)CrossRefGoogle Scholar
  2. 2.
    B.C. Jobst, T.M. Darcey, V.M. Thadani, D.W. Roberts, Epilepsia 51, 88 (2010)CrossRefGoogle Scholar
  3. 3.
    X. Zhang, F. Tokoglu, M. Negishi, J. Arora, S. Winstanley, D.D. Spencer, R.T. Constable, J. Neurosci. Methods 199, 129 (2011)CrossRefGoogle Scholar
  4. 4.
    M. Negishi, R. Martuzzi, E.J. Novotny, D.D. Spencer, R.T. Constable, Epilepsia 52, 1733 (2011)CrossRefGoogle Scholar
  5. 5.
    F. Pittau, C. Grova, F. Moeller, F. Dubeau, J. Gotman, Epilepsia 53, 1013 (2012)CrossRefGoogle Scholar
  6. 6.
    J. Zhang, W. Cheng, Z. Wang, Z. Zhang, W. Lu, G. Lu, J. Feng, PLoS ONE 7, e36733 (2012)ADSCrossRefGoogle Scholar
  7. 7.
    T. Murta, A. Leal, M.I. Garrido, P. Figueiredo, NeuroImage 62, 1642 (2012)CrossRefGoogle Scholar
  8. 8.
    L.D. Iasemidis, J.C. Sackellares, H.P. Zaveri, W.J. Williams, Brain Topogr. 2, 187 (1990)CrossRefGoogle Scholar
  9. 9.
    J.P. Pijn, J. Van Neerven, A.Noest, F.H. Lopes da Silva, Electroencephalogr. Clin. Neurophysiol. 79, 371 (1991)CrossRefGoogle Scholar
  10. 10.
    F.H. Lopes da Silva, J.P. Pijn, W.J. Wadman, Prog. Brain Res. 102, 359 (1994)CrossRefGoogle Scholar
  11. 11.
    K. Lehnertz, C.E. Elger, Electroencephalogr. Clin. Neurophysiol. 95, 108 (1995)CrossRefGoogle Scholar
  12. 12.
    J. Martinerie, C. Adam, M. Le Van Quyen, M. Baulac, S. Clemenceau, B. Renault, F.J. Varela, Nature Med. 4, 1173 (1998)CrossRefGoogle Scholar
  13. 13.
    K.J. Friston, Brain Connectivity 1, 13 (2011)CrossRefGoogle Scholar
  14. 14.
    M.J. Kaminski, K.J. Blinowska, Biol. Cybern. 65, 203 (1991)CrossRefzbMATHGoogle Scholar
  15. 15.
    C.W.J. Granger, Econometrica 37, 424 (1969)CrossRefGoogle Scholar
  16. 16.
    P.J. Franaszczuk, G.K. Bergey, Brain Topogr. 11, 13 (1998)CrossRefGoogle Scholar
  17. 17.
    B. Swiderski, S. Osowski, A. Cichocki, A. Rysz, Neurocomputing 72, 1575 (2009)CrossRefGoogle Scholar
  18. 18.
    C. Wilke, W. van Drongelen, M. Kohrman, B. He, Epilepsia 51, 564 (2010)CrossRefGoogle Scholar
  19. 19.
    P. van Mierlo, E. Carrette, H. Hallez, K. Vonck, D. Van Roost, P. Boon, S. Staelens, NeuroImage 56, 1122 (2011)CrossRefGoogle Scholar
  20. 20.
    A. Korzeniewska, C.M. Crainiceanu, R. Kuś, P.J. Franaszczuk, N.E. Crone, Hum. Brain Mapp. 29, 1170 (2008)CrossRefGoogle Scholar
  21. 21.
    T. Mullen, Z.A. Acar, G. Worrell, S. Makeig, Modeling cortical source dynamics and interactions during seizure, in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vol. 2011 (2011) pp. 1411--4Google Scholar
  22. 22.
    A.J. Bell, T.J. Sejnowski, Neural Comput. 7, 1129 (1995)CrossRefGoogle Scholar
  23. 23.
    L.A. Baccalá, K. Sameshima, Biol. Cybern. 84, 463 (2001)CrossRefzbMATHGoogle Scholar
  24. 24.
    D.Y. Takahashi, L.A. Baccalá, K.Sameshima, J. Appl. Stat. 34, 1259 (2007)MathSciNetCrossRefGoogle Scholar
  25. 25.
    G. Varotto, E. Visani, L. Canafoglia, S. Franceschetti, G. Avanzini, F. Panzica, Epilepsia 53, 359 (2012)CrossRefGoogle Scholar
  26. 26.
    P.J. Franaszczuk, G.K. Bergey, Biol. Cybern. 81, 3 (1999)CrossRefzbMATHGoogle Scholar
  27. 27.
    A.J. Cadotte, T.B. DeMarse, T.H. Mareci, M.B. Parekh, S.S. Talathi, D.-U. Hwang, W.L. Ditto, M. Ding, P.R. Carney, J. Neurosci. Methods 189, 121 (2010)CrossRefGoogle Scholar
  28. 28.
    G.R. Wu, F. Chen, D. Kang, X. Zhang, D. Marinazzo, H. Chen, IEEE Trans. Biomed. Eng. 58, 3088 (2011)CrossRefGoogle Scholar
  29. 29.
    H. Akaike, IEEE Trans. Autom. Control 19, 716 (1974)MathSciNetADSCrossRefzbMATHGoogle Scholar
  30. 30.
    G. Schwarz, Ann. Stat.s 6, 461 (1978)CrossRefzbMATHGoogle Scholar
  31. 31.
    B.G. Quinn, J. R. Stat. Soc. Ser. B 42, 182 (1980)MathSciNetzbMATHGoogle Scholar
  32. 32.
    R. Kohavi, A Study of Cross-Validation and Bootstrap for Accuracy Estimation and Model Selection, in IJCAI-95: Proceedings of the 14th International Joint Conference on Artificial Intelligence, Vol. 2 (Morgan Kaufmann Publishers Inc., San Francisco, 1995) pp. 1137--1143Google Scholar
  33. 33.
    S. Spencer, Epilepsia 43, 219 (2002)CrossRefGoogle Scholar
  34. 34.
    S.C. Ponten, F. Bartolomei, C.J. Stam, Clin. Neurophysiol. 118, 918 (2007)CrossRefGoogle Scholar
  35. 35.
    M.A. Kramer, E.D. Kolaczyk, H.E. Kirsch, Epilepsy Res. 79, 173 (2008)CrossRefGoogle Scholar
  36. 36.
    F. Wendling, P. Chauvel, A. Biraben, F. Bartolomei, Front. Syst. Neurosci. 4, 154 (2010)CrossRefGoogle Scholar
  37. 37.
    J.R. Terry, O. Benjamin, M.P. Richardson, Epilepsia 53, e166 (2012) DOI:10.1111/j.1528-1167.2012.03560.x CrossRefGoogle Scholar
  38. 38.
    K. Lehnertz, C. Elger, Phys. Rev. Lett. 80, 5019 (1998)ADSCrossRefGoogle Scholar
  39. 39.
    F. Mormann, K. Lehnertz, P. David, C.E. Elger, Physica D 144, 358 (2000)ADSCrossRefzbMATHGoogle Scholar
  40. 40.
    B. Litt, J. Echauz, Lancet Neurology 1, 22 (2002)CrossRefGoogle Scholar
  41. 41.
    F. Mormann, R.G. Andrzejak, T. Kreuz, C. Rieke, P. David, C.E. Elger, K. Lehnertz, Phys. Rev. E 67, 021912 (2003)ADSCrossRefGoogle Scholar
  42. 42.
    M. Winterhalder, B. Schelter, T. Maiwald, A. Brandt, A. Schad, A. Schulze-Bonhage, J. Timmer, Clin. Neurophysiol. 117, 2399 (2006)CrossRefGoogle Scholar
  43. 43.
    I. Osorio, Y.-C. Lai, Chaos (N.Y.) 21, 033108 (2011)ADSCrossRefGoogle Scholar
  44. 44.
    G. Ouyang, X. Li, Y. Li, X. Guan, Comput. Biol. Med. 37, 430 (2007)CrossRefGoogle Scholar
  45. 45.
    R.G. Andrzejak, D. Chicharro, C.E. Elger, F. Mormann, Clin. Neurophysiol. 120, 1465 (2009)CrossRefGoogle Scholar
  46. 46.
    M.S.D. Kerr, S.P. Burns, J. Gale, J. Gonzalez-Martinez, J. Bulacio, S.V. Sarma, Multivariate analysis of SEEG signals during seizure, in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vol. 2011 (2011) pp. 8279--8282Google Scholar
  47. 47.
    S. Santaniello, S.P. Burns, A.J. Golby, J.M. Singer, W.S. Anderson, S.V. Sarma, Epilepsy Behav. 22, S49 (2011)CrossRefGoogle Scholar
  48. 48.
    L.D. Iasemidis, D.-S. Shiau, J.C. Sackellares, P.M. Pardalos, A. Prasad, IEEE Trans. Biomed. Eng. 51, 493 (2004)CrossRefGoogle Scholar
  49. 49.
    M. Chávez, M. Le Van Quyen, V. Navarro, M. Baulac, J. Martinerie, IEEE Trans. Biomed. Eng. 50, 571 (2003)CrossRefGoogle Scholar
  50. 50.
    M. Palus, V. Komárek, Z. Hrncír, K. Sterbová, Phys. Rev. E 63, 046211 (2001)ADSCrossRefGoogle Scholar
  51. 51.
    M. Eichler, Biol. Cybern. 94, 469 (2006)MathSciNetCrossRefzbMATHGoogle Scholar
  52. 52.
    D.Y. Takahashi, L.A. Baccalá, K. Sameshima, Biol. Cybern. 103, 463 (2010)CrossRefGoogle Scholar
  53. 53.
    L. Barnett, A.B. Barrett, A.K. Seth, Phys. Rev. Lett. 103, 238701 (2009)ADSCrossRefGoogle Scholar
  54. 54.
    T. Schreiber, Phys. Rev. Lett. 85, 461 (2000)ADSCrossRefGoogle Scholar
  55. 55.
    D. Marinazzo, M. Pellicoro, S. Stramaglia, Computational and Mathematical Methods in Medicine 2012, 303601 (2012)MathSciNetCrossRefGoogle Scholar
  56. 56.
    S. Sabesan, L.B. Good, K.S. Tsakalis, A. Spanias, D.M. Treiman, L.D. Iasemidis, IEEE transactions on neural systems and rehabilitation engineering 17, 244 (2009)CrossRefGoogle Scholar
  57. 57.
    C. Stamoulis, B.S. Chang, Multiscale information for network characterization in epilepsy, in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vol. 2011 (2011) pp. 5908--11Google Scholar
  58. 58.
    C. Stamoulis, L.J. Gruber, D.L. Schomer, B.S. Chang, Epilepsy Behav. 23, 471 (2012)CrossRefGoogle Scholar
  59. 59.
    M. Lindner, R. Vicente, V. Priesemann, M. Wibral, BMC Neurosci. 12, 119 (2011)CrossRefGoogle Scholar
  60. 60.
    J. Geweke, J. Am. Stat. Assoc. 77, 304 (1982)MathSciNetCrossRefzbMATHGoogle Scholar
  61. 61.
    E. Florin, J. Gross, J. Pfeifer, G.R. Fink, L. Timmermann, NeuroImage 50, 577 (2010)CrossRefGoogle Scholar
  62. 62.
    L. Barnett, A.K. Seth, J. Neurosci. Methods 201, 404 (2011)CrossRefGoogle Scholar
  63. 63.
    A. Korzeniewska, M. Mańczak, M. Kamiński, K.J. Blinowska, S. Kasicki, J. Neurosci. Methods 125, 195 (2003)CrossRefGoogle Scholar
  64. 64.
    M. Kamiński, Phil. Trans. R. Soc. London. Ser. B Biol. Sci. 360, 947 (2005)CrossRefGoogle Scholar
  65. 65.
    L. Faes, G. Nollo, Assessing directional interactions among multiple physiological time series: the role of instantaneous causality, in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vol. 2011 (2011) pp. 5919--5922Google Scholar
  66. 66.
    K.J. Blinowska, Med. Biol. Eng. Comput. 49, 521 (2011)CrossRefGoogle Scholar
  67. 67.
    D. Marinazzo, G. Wu, M. Pellicoro, L. Angelini, S. Stramaglia, PLoS ONE 7, e45026 (2012)ADSCrossRefGoogle Scholar
  68. 68.
    J.X. Tao, M. Baldwin, A. Ray, S. Hawes-Ebersole, J.S. Ebersole, Epilepsia 48, 2167 (2007)CrossRefGoogle Scholar

Copyright information

© Società Italiana di Fisica and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Margarita Papadopoulou
    • 1
  • Kristl Vonck
    • 2
  • Paul Boon
    • 2
  • Daniele Marinazzo
    • 1
    Email author
  1. 1.Department of Data Analysis, Faculty of Psychology and Pedagogical SciencesGhent UniversityGhentBelgium
  2. 2.Laboratory for Clinical and Experimental NeurophysiologyGhent University HospitalGhentBelgium

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