Synchrony in normal and focal epileptic brain: The seizure onset zone is functionally disconnected

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3530-3539

  Warren, Christopher P ^a   Hu, Sanqing ^a,b   Stead, Matt ^a   Brinkmann, Benjamin H ^a   Bower, Mark R ^a   Worrell, Gregory A ^a  

^a MAYO CLINIC   (United States)

^b HANGZHOU DIANZI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN FUNCTION; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EPILEPSY; HUMAN; PRIORITY JOURNAL; SEIZURE;

ALGORITHMS; BRAIN NEOPLASMS; CORTICAL SYNCHRONIZATION; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; EPENDYMOMA; EPILEPSIES, PARTIAL; FACIAL PAIN; HUMANS; MALFORMATIONS OF CORTICAL DEVELOPMENT; MOTOR CORTEX; NEURAL PATHWAYS;

EID: 78650910997     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00368.2010     Document Type: Article

References (66)

1. Aarabi A, Wallois F, Grebe R. Does spatiotemporal synchronization of EEG change prior to absence seizures? Brain Res 1188: 207-211, 2007.
2. Alper K, Raghavan M, Isenhart R, Howard B, Doyle W, John R, Prichep L. Localizing epileptogenic regions in partial epilepsy using three-dimensional statistical parametric maps of background EEG source spectra. Neuroimage 39: 1257-1265, 2008.
3. Amor F, Rudrauf D, Navarro V, N'diaye K, Garnero L, Martinerie J, Le Van Quyen M. Imaging brain synchrony at high spatio-temporal resolution: Application to MEG signals during absence seizures. Signal Processing 85: 2101-2111, 2005.
4. Ansari-Asl K, Senhadji L, Bellanger JJ, Wendling F. Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. Phys Rev E Stat Nonlin Soft Matter Phys 74: 031916, 2006.
5. Avramescu S, Nita DA, Timofeev I. Neocortical post-traumatic epileptogenesis is associated with loss of GABAergic neurons. J Neurotrauma 26: 799-812, 2009.
6. Avramescu S, Timofeev I. Synaptic strength modulation after cortical trauma: A role in epileptogenesis. J Neurosci 28: 6760-6772, 2008.
7. Bartlett MS. On the theoretical specification and sampling properties of autocorrelated time-series. J R Stati Soc B 8: 27-41, 1946.
8. Bartolomei F, Wendling F, Bellanger JJ, Régis J, Chauvel P. Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol 112: 1746-1760, 2001.
9. Bettus G, Wendling F, Guye M, Valton L, Régis J, Chauvel P, Bartolomei F. Enhanced EEG functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res 81: 58-68, 2008.
10. Blumenfeld H, McNally KA, Vanderhill SD, Paige AL, Chung R, Davis K, Norden AD, Stokking R, Studholme C, Novotny EJ, Zubal IG, Spencer SS. Positive and negative network correlations in temporal lobe epilepsy. Cereb Cortex 14: 892-902, 2004.
11. Bower MR, Buckmaster PS. Changes in granule cell firing rates precede locally recorded spontaneous seizures by minutes in an animal model of temporal lobe epilepsy. J Neurophysiol 99: 2431-2442, 2008.
12. Brinkmann BH, Bower MR, Stengel KA, Worrell GA, Stead M. Largescale electrophysiology: Acquisition, compression, encryption, and storage of big data. J Neurosci Methods 180: 185-192, 2009.
13. Bullmore E, Sporns O. Complex brain networks: Graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10: 186-198, 2009.
14. Cymerblit-Sabba A, Schiller Y. Network dynamics during development of pharmacologically induced epileptic seizures in rats in vivo. J Neurosci 30: 1619-1630, 2010.
15. David O, Cosmelli D, Friston KJ. Evaluation of different measures of functional connectivity using a neural mass model. Neuroimage 21: 659-673, 2004.
16. Doesburg SM, Ward LM. Synchronization between sources: Emerging methods for understanding large-scale Functional networks in the human brain. In: Coordinated Activity in the Brain: Measurements and Relevance to Brain Function and Behavior. New York: Springer, 2009 p. 25-42.
17. Elger CE, Lehnertz K. Seizure prediction by non-linear time series analysis of brain electrical activity. Eur J Neurosci 10: 786-789, 1998.
18. Engel AK, Moll CK, Fried I, Ojemann GA. Invasive recordings from the human brain: Clinical insights and beyond. Nat Rev Neurosci 6: 35-47, 2005.
19. Faingold CL. Emergent properties of CNS neuronal networks as targets for pharmacology: Application to anticonvulsant drug action. Prog Neurobiol 72: 55-85, 2004.
20. Golomb D. Models of neuronal transient synchrony during propagation of activity through neocortical circuitry. J Neurophysiol 79: 1-12, 1998.
21. Guevara R, Velazquez JLP, Nenadovic V, Wennberg R, Senjanović G, Dominguez LG. Phase synchronization measurements using electroencephalographic recordings. Neuroinformatics 3: 301-313, 2005.
22. Gutkin BS, Laing CR, Colby CL, Chow CC, Ermentrout GB. Turning on and off with excitation: The role of spike-timing asynchrony and synchrony in sustained neural activity. J Comput Neurosci 11: 121-134, 2001.
23. Horwitz B. The elusive concept of brain connectivity. Neuroimage 19: 466-470, 2003.
24. Houweling AR, Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb Cortex 15: 834-845, 2005.
25. Hu S, Stead M, Dai Q, Worrell GA. On the recording reference contribution to EEG correlation, phase synchrony, and coherence. IEEE Trans Syst Man Cybern B Cybern, 40: 1294-1304, 2010.
26. Iasemidis LD, Sackellares JC, Zaveri HP, Williams WJ. Phase space topography and the Lyapunov exponent of electrocorticograms in partial seizures. Brain Topogr 2: 187-201, 1990.
27. Jasper H, Penfield WG. Epilepsy and the Functional Anatomy of the Human Brain. Boston, MA: Little, Brown, 1954.
28. Ken S, Di Gennaro G, Giulietti G, Sebastiano F, De Carli D, Garreffa G, Colonnese C, Passariello R, Lotterie JA, Maraviglia B. Quantitative evaluation for brain CT/MRI coregistration based on maximization of mutual information in patients with focal epilepsy investigated with subdural electrodes. Magn Reson Imaging 25: 883-888, 2007.
29. Kramer MA, Kolaczyk ED, Kirsch HE. Emergent network topology at seizure onset in humans. Epilepsy Res 79: 173-186, 2008.
30. Le Van Quyen M, Adam C, Baulac M, Martinerie J, Varela FJ. Nonlinear interdependencies of EEG signals in human intracranially recorded temporal lobe seizures. Brain Res 792: 24-40, 1998.
31. Le Van Quyen M, Adam C, Martinerie J, Baulac M, Clémenceau S, Varela F. Spatio-temporal characterizations of non-linear changes in intracranial activities prior to human temporal lobe seizures. Eur J Neurosci 12: 2124-2134, 2000.
32. Le Van Quyen M, Martinerie J, Baulac M, Varela F. Anticipating epileptic seizures in real time by a non-linear analysis of similarity between EEG recordings. Neuroreport 10: 2149-2155, 1999.
33. Le Van Quyen M, Martinerie J, Navarro V, Boon P, D'Havé M, Adam C, Renault B, Varela F, Baulac M. Anticipation of epileptic seizures from standard EEG recordings. Lancet 357: 183-188, 2001.
34. Liang F, Le LD, Jones EG. Reciprocal up- and down-regulation of BDNF mRNA in tetanus toxin-induced epileptic focus and inhibitory surround in cerebral cortex. Cereb Cortex 8: 481-491, 1998.
35. Lima MC, Fregni F. Motor cortex stimulation for chronic pain: Systematic review and meta-analysis of the literature. Neurology 70: 2329-2337, 2008.
36. Logothetis NK, Kayser C, Oeltermann A. In vivo measurement of cortical impedance spectrum in monkeys: Implications for signal propagation. Neuron 55: 809-823, 2007.
37. Lopes da Silva FH, Blanes W, Kalitzin SN, Parra J, Suffczynski P, Velis DN. Dynamical diseases of brain systems: Different routes to epileptic seizures. IEEE Trans Biomed Eng 50: 540-548, 2003.
38. Martinerie J, Adam C, Le Van Quyen M, Baulac M, Clemenceau S, Renault B, Varela FJ. Epileptic seizures can be anticipated by non-linear analysis. Nat Med 4: 1173-1176, 1998.
39. McCormick DA, Contreras D. On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63: 815-846, 2001.
40. Mitzdorf U. Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiol Rev 65: 37-100, 1985.
41. Mormann F, Elger CE, Lehnertz K. Seizure anticipation: From algorithms to clinical practice. Curr Opin Neurol 19: 187-193, 2006.
42. Mormann F, Lehnertz K, David P, Elger CE. Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Phys D: Nonlinear Phenomena 144: 358-369, 2000.
43. Netoff TI, Schiff SJ. Decreased neuronal synchronization during experimental seizures. J Neurosci 22: 7297-7307, 2002.
44. Pan JW, Kim JH, Cohen-Gadol A, Pan C, Spencer DD, Hetherington HP. Regional energetic dysfunction in hippocampal epilepsy. Acta Neurol Scand 111: 218-224, 2005.
45. Perez Velazquez JL, Guevara Erra R, Wennberg R, Dominquez LG. Correlations of cellular activities in the nervous system: Physiological and methodological considerations, In: Coordinated Activity in the Brain: Measurements and Relevance to Brain Function and Behavior. New York: Springer, 2009 p. 1-24.
46. Prince DA, Wilder BJ. Control mechanisms in cortical epileptogenic foci. "Surround" inhibition. Arch Neurol 16: 194-202, 1967.
47. Rulkov NF, Sushchik MM, Tsimring LS, Abarbanel HD. Generalized synchronization of chaos in directionally coupled chaotic systems. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 51: 980-994, 1995.
48. Schevon CA, Cappell J, Emerson R, Isler J, Grieve P, Goodman R, McKhann G, Weiner H, Doyle W, Kuzniecky R, Devinsky O, Gilliam F. Cortical abnormalities in epilepsy revealed by local EEG synchrony. Neuroimage 35: 140-148, 2007.
49. Schiff SJ. Dangerous phase. Neuroinformatics 3: 315-318, 2005.
50. Schindler K, Elger CE, Lehnertz K. Increasing synchronization may promote seizure termination: Evidence from status epilepticus. Clin Neurophysiol 118: 1955-1968, 2007.
51. Schindler KA, Bialonski S, Horstmann MT, Elger CE, Lehnertz K. Evolving functional network properties and synchronizability during human epileptic seizures. Chaos 18: 033119, 2008.
52. Spencer SS. Neural networks in human epilepsy: Evidence of and implications for treatment. Epilepsia 43: 219-227, 2002.
53. Stead M, Bower MR, Brinkmann BH, Lee K, Marsh WR, Meyer FB, Litt B, Van Gompel J, Worrell GA. Microseizures and the spatiotemporal scales of human partial epilepsy. Brain 133: 2789-2797, 2010.
54. Stephan KE, Riera JJ, Deco G, Horwitz B. The Brain Connectivity Workshops: Moving the frontiers of computational systems neuroscience. Neuroimage 42: 1-9, 2008.
55. Sun J, Small M. Unified framework for detecting phase synchronization in coupled time series. Phys Rev E Stat Nonlin Soft Matter Phys 80: 046219, 2009.
56. Tao JX, Ray A, Hawes-Ebersole S, Ebersole JS. Intracranial EEG substrates of scalp EEG interictal spikes. Epilepsia 46: 669-676, 2005.
57. Towle VL, Carder RK, Khorasani L, Lindberg D. Electrocorticographic coherence patterns. J Clin Neurophysiol 16: 528-547, 1999.
58. Towle VL, Syed I, Berger C, Grzesczcuk R, Milton J, Erickson RK, Cogen P, Berkson E, Spire JP. Identification of the sensory/motor area and pathologic regions using ECoG coherence. Electroencephalogr Clin Neurophysiol 106: 30-39, 1998.
59. Van Gompel JJ, Stead SM, Giannini C, Meyer FB, Marsh WR, Fountain T, So E, Cohen-Gadol A, Lee KH, Worrell GA. Phase I trial: Safety and feasibility of intracranial electroencephalography using hybrid subdural electrodes containing macro- and microelectrode arrays. Neurosurg Focus 25: E23, 2008.
60. Wendling F, Bartolomei F, Bellanger JJ, Bourien J, Chauvel P. Epileptic fast intracerebral EEG activity: Evidence for spatial decorrelation at seizure onset. Brain 126: 1449, 2003.
61. Wetjen NM, Marsh WR, Meyer FB, Cascino GD, So E, Britton JW, Stead SM, Worrell GA. Intracranial electroencephalography seizure onset patterns and surgical outcomes in nonlesional extratemporal epilepsy. J Neurosurg 110: 1147-1152, 2009.
62. Worrell GA, Gardner AB, Stead SM, Hu S, Goerss S, Cascino GJ, Meyer FB, Marsh R, Litt B. High-frequency oscillations in human temporal lobe: Simultaneous microwire and clinical macroelectrode recordings. Brain 131: 928-937, 2008.
63. Worrell GA, Parish L, Cranstoun SD, Jonas R, Baltuch G, Litt B. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 127: 1496-1506, 2004.
64. Zaveri HP, Duckrow RB, Spencer SS. The effect of a scalp reference signal on coherence measurements of intracranial electroencephalograms. Clin Neurophysiol 111: 1293-1299, 2000.
65. Zaveri HP, Pincus SM, Goncharova II, Duckrow RB, Spencer DD, Spencer SS. Localization-related epilepsy exhibits significant connectivity away from the seizure-onset area. Neuroreport 20: 891-895, 2009.
66. Zeng LH, Xu L, Rensing NR, Sinatra PM, Rothman SM, Wong M. Kainate seizures cause acute dendritic injury and actin depolymerization in vivo. J Neurosci 27: 11604-11613, 2007.