Epileptic seizures from abnormal networks: Why some seizures defy predictability

Epilepsy Research

Volumn 99, Issue 3, 2012, Pages 202-213

  Anderson, William S ^a   Azhar, Feraz ^a   Kudela, Pawel ^a   Bergey, Gregory K ^a   Franaszczuk, Piotr J ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b U S ARMY RESEARCH LABORATORY   (United States)

Author keywords

Computational simulation; Neural network model; Seizure generation; Seizure prediction

Indexed keywords

ACTION POTENTIAL; ARTICLE; ARTIFICIAL NEURAL NETWORK; FOCAL EPILEPSY; GAMMA DISTRIBUTION; HUMAN; INTERBURSTING PHASE INTERVAL; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE POTENTIAL; NONPARAMETRIC TEST; PERIODICITY; POISSON DISTRIBUTION; PREDICTION; PRIORITY JOURNAL; PROBABILITY; SEIZURE; STATISTICAL ANALYSIS;

CEREBRAL CORTEX; COMPUTER SIMULATION; EPILEPSY; NEURAL NETWORKS (COMPUTER); PREDICTIVE VALUE OF TESTS; PYRAMIDAL CELLS; RANDOM ALLOCATION;

EID: 84860450169     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2011.11.006     Document Type: Article

References (63)

1. Afra P., Jouny C.C., Bergey G.K. Duration of complex partial seizures: an intracranial EEG study. Epilepsia 2008, 49(4):677-684.
2. Anderson W.S., Kudela P., Cho R.J., Bergey G.K., Franaszczuk P. Studies of stimulus parameters for seizure disruption using neural network simulations. Biol. Cybern. 2007, 97:173-194.
3. Anderson W.S., Weinberg S., Kudela P., Bergey G.K., Franaszczuk P. Phase dependent stimulation effects on bursting activity in a neural network cortical simulation. Epilepsy Res. 2009, 84:42-55.
4. Andrzejak R.G., Chicharro D., Elger C.E., Mormann F. Seizure prediction: any better than chance?. Clin. Neurophysiol. 2009, 120(8):1465-1478.
5. Arellano J.I., Muñoz A., Ballesteros-Yáñez I., Sola R.G., DeFelipe J. Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain 2004, 127:45-64.
6. Av-Ron E. The role of a transient potassium current in a bursting neuron model. J. Math. Biol. 1994, 33:71-87.
7. Berg A.T., Shinnar S. The risk of seizure recurrence following a first unprovoked seizure: a quantitative review. Neurology 1991, 41:965-972.
8. Bragin A., Engel J., Staba R.J. High-frequency oscillations in epileptic brain. Curr. Opin. Neurol. 2010, 23(2):151-156.
9. Braitenberg V., Schüz A. Cortex: Statistics and Geometry of Neuronal Connectivity 1998, Springer, Berlin. 2nd edition.
10. Dinocourt C., Petanjek Z., Freund T.F., Ben-Ari Y., Esclapez M. Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J. Comp. Neurol. 2003, 459:407-425.
11. Douglas R.J., Martin K.A.C. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 2004, 27:419-451.
12. Dudek F.E., Sutula T.P. Epileptogenesis in the dentate gyrus: a critical perspective. Prog. Brain Res. 2007, 163. 755-753.
13. Dyhrfjeld-Johnsen J., Santhakumar V., Morgan R.J., Huerta R., Tsimring L., Soltesz I. Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J. Neurophysiol. 2007, 97(2):1566-1587.
14. Estellar R., Echauz J., Tcheng T., Litt B., Pless B. Line length: an efficient feature of seizure onset detection. Proc 23rd Annu Int Conf IEEE Eng Med Biol Soc 2001, 1707-1710.
15. Farkhooi F., Strube-Bloss M.F., Nawrot M.P. Serial correlation in neural spike trains, experimental evidence, stochastic modeling, and single neuron variability. Phys. Rev. E: Stat. Nonlin. Soft Matter Phys. 2009, 79:021905.
16. Franaszczuk P.J., Kudela P., Bergey G.K. External excitatory stimuli can terminate bursting in neural network models. Epilepsy Res. 2003, 53:65-80.
17. Guckenheimer J., Holmes P. Nonlinear Oscillations, Dynamical Systems, and Bifurcations of Vector Fields 1983, Springer-Verlag, New York.
18. Haas S.M., Frei M.G., Osorio I. Strategies for adapting automated seizure detection algorithms. Med. Eng. Phys. 2007, 29(8):895-909.
19. Hauser W.A., Annegers J.F., Kurland L.T. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935-1984. Epilepsia 1993, 34:453-468.
20. Hegyi S. Multiplicity distributions in strong interactions: a generalized negative binomial model. Phys. Lett. B 1996, 387:642-650.
21. Jacobs K.M., Graber K.D., Kharazia V.N., Parada I., Prince D.A. Postlesional epilepsy: the ultimate brain plasticity. Epilepsia 2000, 41(Suppl. 6):S153-S161.
22. Kaplan Y., Kurt S.G., Karaer H., Sarikaya B., Bebek N. Intra-familial incidence and characteristics of hot water epilepsy. Can. J. Neurol. Sci. 2009, 36(5):575-581.
23. Keefer E.W., Gramowski A., Gross G.W. NMDA receptor-dependent periodic oscillations in cultured spinal cord networks. J. Neurophysiol. 2001, 86:3030-3042.
24. Kowalski J.M., Albert G.L., Rhoades B.K., Gross G.W. Neuronal networks with spontaneous, correlated bursting activity: theory and simulations. Neural Netw. 1992, 5:805-822.
25. Krumholz A., Wiebe S., Gronseth G., Shinnar S., Levisohn P., Ting T., Hopp J., Shafer P., Morris H., Seiden L., Barkley G., French J. Practice parameter: evaluating an apparent unprovoked first seizure in adults (an evidence-based review). Report of the quality standards subcommittee of the American Academy of Neurology and the American Epilepsy Society. Neurology 2007, 69:1996-2007.
26. Kudela P., Franaszczuk P.J., Bergey G.K. A simple computer model of excitable synaptically connected neurons. Biol. Cybern. 1997, 77:71-77.
27. Kudela P., Franaszczuk P.J., Bergey G.K. Changing excitation and inhibition in simulated neural networks: effects on induced bursting behavior. Biol. Cybern. 2003, 88:276-285.
28. Kudela P., Franaszczuk P., Bergey G.K. Reduction of intracellular calcium removal rate can explain changes in seizure dynamics: studies in neuronal network models. Epilepsy Res. 2003, 57:95-109.
29. Kudela P., Franaszczuk P.J., Bergey G.K. Synaptic and cellular influences on the composite EEG signal during seizures. Proc 2nd Inter IEEE EMBS Conf Neural Eng 2005, 245-247. IEEE, Arlington, VA.
30. Kumar S.S., Jin X., Buckmaster P.S., Huguenard J.R. Recurrent circuits in layer II of medial entorhinal cortex in a model of temporal lobe epilepsy. J. Neurosci. 2007, 27:1239-1246.
31. Lehnertz K., Mormann F., Osterhage H., Müller A., Prusseit J., Chernihovskyi A., Staniek M., Krug D., Bialonski S., Elger C.E. State-of-the-art of seizure prediction. J. Clin. Neurophysiol. 2007, 24(2):147-153.
32. Leussis M.P., Heinrichs S.C. Temporal ontogeny of circuit activation prior to the onset of seizure susceptibility in EL/Suz mice. Neuroscience 2007, 145:33-41.
33. Le Van Quyen M., Martinerie J., Adam C., Varela F.J. Unstable periodic orbits in human epileptic activity. Phys. Rev. E 1997, 56(3):3401-3411.
34. Litt B., Echauz J. Prediction of epileptic seizures. Lancet Neurol. 2002, 1:22-30.
35. Lopes da Silva F., Blanes W., Kalitzin S.N., Parra J., Suffczynski P., Velis D.N. Epilepsies as dynamical diseases of brain systems: basic models of the transition between normal and epileptic activity. Epilepsia 2003, 44(Suppl. 12):72-83.
36. Lu Y., Waltz S., Stenzel K., Muhle H., Stephani U. Photosensitivity in epileptic syndromes of childhood and adolescence. Epileptic Disord. 2008, 10(2):144-145.
37. Maglóscky Z. Sprouting in human temporal lobe epilepsy: excitatory pathways and axons of interneurons. Epilepsy Res. 2010, 89:52-59.
38. Marco P., Sola R.G., Rámon y Cajal S., DeFelipe J. Loss of inhibitory synapses on the soma and axon initial segment of pyramidal cells in human epileptic peritumoural neocortex: implications for epilepsy. Brain Res. Bull. 1997, 44:47-66.
39. Morgan R.J., Soltesz I. Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc. Natl. Acad. Sci. U.S.A. 2008, 105(16):6179-6184.
40. Mormann F., Andrzejak R.G., Elger C.E., Lehnertz K. Seizure prediction: the long and winding road. Brain 2007, 130:314-333.
41. Niedermeyer E. Epileptic seizure disorders. Electroencephalography 2005, 505-619. Lippincott Williams & Wilkins, Philadelphia. 5th edition. E. Niedermeyer, F. Lopes da Silva (Eds.).
42. Osorio I., Frei M.G., Manly B.F.J., Sunderam S., Bhavaraju N.C., Wilkinson S.B. An introduction to contingent (closed-loop) brain electrical stimulation for seizure blockage, ultra-short-term clinical trials, and to multidimensional statistical analysis of therapeutic efficacy. J. Clin. Neurophysiol. 2001, 18(6):533-544.
43. Osorio I., Frei M.G., Sornette D., Milton J. Pharmaco-resistant seizures: self-triggering capacity, scale-free properties and predictability?. Eur. J. Neurosci. 2009, 30:1554-1558.
44. Osorio I., Frei M.G., Sornette D., Milton J., Lai Y.-C. Epileptic seizures: quakes of the brain?. Phys. Rev. E 2010, 82:021919.
45. Papoulis A. Probability, Random Variables, and Stochastic Processes 1984, McGraw-Hill, New York. 2nd edition.
46. Rhoades B.K., Gross G.W. Potassium and calcium channel dependence of bursting in cultured neuronal networks. Brain Res. 1994, 643:310-318.
47. Sackellares J.C., Shiau D.S., Principe J.C., Yang M.C., Dance L.K., Suharitdamrong W., Chaovalitwongse W., Pardalos P.M., Iasemidis L.D. Predictability analysis for an automated seizure prediction algorithm. J. Clin. Neurophysiol. 2006, 23:509-520.
48. Sackellares J.C. Seizure prediction. Epilepsy Curr. 2008, 8(3):55-59.
49. Sallin P., Tseng G.-F., Hoffman S., Parada I., Prince D.A. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J. Neurosci. 1995, 15(12):8234-8245.
50. So P., Ott E., Schiff S.J., Kaplan D.T., Sauer T., Grebogi C. Detecting unstable periodic orbits in chaotic experimental data. Phys. Rev. Lett. 1996, 76(25):4705-4708.
51. So P., Ott E., Sauer T., Gluckman B.J., Grebogi C., Schiff S.J. Extracting unstable periodic orbits from chaotic time series data. Phys. Rev. E 1997, 55(5):5398-5417.
52. Suffczynski P., Lopes da Silva F., Parra J., Velis D., Kalitzin S. Epileptic transitions: model predictions and experimental validation. J. Clin. Neurophysiol. 2005, 22(5):288-299.
53. Suffczynski P., Lopes da Silva F.H., Parra J., Velis D.N., Bouwman B.M., van Rijn C.M., van Hese P., Boon P., Khosravani H., Derchansky M., Carlen P., Kalitzin S. Dynamics of epileptic phenomena determined from statistics of ictal transitions. IEEE Trans. Biomed. Eng. 2006, 53(3):524-532.
54. Swann J.W., Le J.T., Lee C.L. Recurrent seizures and the molecular maturation of hippocampal and neocortical glutamatergic synapses. Dev. Neurosci. 2007, 29:168-178.
55. Telfeian A.E., Connors B.W. Layer-specific pathways for the horizontal propagation of epileptiform discharges in neocortex. Epilepsia 1998, 39:700-708.
56. Theiler J., Eubank S., Longtin A., Galdrikian B., Farmer J.D. Testing for nonlinearity in time series: the method of surrogate data. Physica D 1992, 58:77-94.
57. Truccolo W., Donoghue J., Hochberg L., Eskandar E., Madsen J.R., Anderson W.S., Halgren E., Cash S.S. Single neuron dynamics during human focal seizures. Nat. Neurosci. 2011, 14(5):635-641.
58. van Gompel J.J., Stead S.M., Giannini C., Meyer F.B., Marsh W.R., Fountain T., So E., Cohen-Gadol A., Lee K.H., Worrell G.A. Phase I trial: safety and feasibility of intracranial electroencephalography using hybrid subdural electrodes containing macro- and microelectrode arrays. Neurosurg. Focus 2008, 25(3):E23.
59. Vinogradova L.V., Kuznetsova G.D., Coenen A.M. Unilateral cortical spreading depression induced by sound in rats. Brain Res. 2009, 1286:201-207.
60. Wald A., Wolfowitz J. An exact test for randomness in the non-parametric case based on serial correlation. Ann. Math. Stat. 1943, 14(4):378-388.
61. Waters J., Helmchen F. Background synaptic activity is sparse in neocortex. J. Neurosci. 2006, 26(32):8267-8277.
62. Worrell G.A., Gardner A.B., Stead S.M., Hu S., Goerss S., Cascino G.J., Meyer F.B., Marsh R., Litt B. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain 2008, 131(Pt 4):928-937.
63. Worrell G.A., Parish L., Cranstoun S.D., Jonas R., Baltuch G., Litt B. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 2004, 127(Pt 7):1496-1506.