Dynamics of high-frequency synchronization during seizures

Journal of Neurophysiology

Volumn 109, Issue 10, 2013, Pages 2423-2437

  Krishnan, Giri P ^a   Filatov, Gregory ^a   Bazhenov, Maxim ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epilepsy; High frequency activity; Seizure; Synchrony

Indexed keywords

POTASSIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; EPILEPTIC DISCHARGE; EXTRACELLULAR POTASSIUM; EXTRACELLULAR SPACE; HIPPOCAMPUS; HYPERPOLARIZATION; IN VITRO STUDY; MOUSE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEIZURE; SPATIAL ORIENTATION; SPATIOTEMPORAL ANALYSIS; SPECTROSCOPY; STRATUM PYRAMIDALE; STRATUM RADIATUM;

EID: 84878606310     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00761.2012     Document Type: Article

References (72)

1. Adhikari A, Sigurdsson T, Topiwala MA, Gordon JA. Cross-correlation of instantaneous amplitudes of field potential oscillations: a straightforward method to estimate the directionality and lag between brain areas. J Neurosci Methods 191: 191-200, 2010.
2. Akin M. Comparison of wavelet transform and FFT methods in the analysis of EEG signals. J Med Syst 26: 241-247, 2002.
3. Anastassiou CA, Montgomery SM, Barahona M, Buzsáki G, Koch C. The effect of spatially inhomogeneous extracellular electric fields on neurons. J Neurosci 30: 1925-1936, 2010.
4. Anderson WW, Lewis DV, Swartzwelder HS, Wilson WA. Magnesium-free medium activates seizure-like events in the rat hippocampal slice. Brain Res 398: 215-219, 1986.
5. Avoli M, Psarropoulou C, Tancredi V, Fueta Y. On the synchronous activity induced by 4-aminopyridine in the CA3 subfield of juvenile rat hippocampus. J Neurophysiol 70: 1018-1029, 1993.
6. Azad AK, Ashwin P. Within-burst synchrony changes for coupled elliptic bursters. SIAM J Imaging Sci 3: 261281, 2010.
7. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Potassium models for slow (2-3 Hz) in vivo neocortical paroxysmal oscillations. J Neurophysiol 92: 1116-1132, 2004.
8. Bazhenov M, Timofeev I, Fröhlich F, Sejnowski TJ. Cellular and network mechanisms of electrographic seizures. Drug Discov Today Dis Models 5: 45-57, 2008.
9. Belluscio MA, Mizuseki K, Schmidt R, Kempter R, Buzsáki G. Cross-frequency phase-phase coupling between and oscillations in the hippocampus. J Neurosci 32: 423-435, 2012.
10. Bragin A, Csicsvari J, Penttonen M, Buzsáki G. Epileptic afterdischarge in the hippocampal-entorhinal system: current source density and unit studies. Neuroscience 76: 1187-1203, 1997.
11. Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus 9: 137-142, 1999a.
12. Bragin A, Engel J Jr, Wilson CL, Fried I, Mathern GW. Hippocampal and entorhinal cortex high-frequency oscillations (100-500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 40: 127-137, 1999b.
13. Bragin A, Wilson CL, Engel J Jr. Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia, 41 Suppl6: S144-S152, 2000.
14. Buzsáki G. Hippocampal sharp waves: their origin and significance. Brain Res 398: 242-252, 1986.
15. Buzsáki G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31: 551-570, 1989.
16. Buzsáki G, Silva FL. High frequency oscillations in the intact brain. Prog Neurobiol 98: 241-249, 2012.
17. Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science 256: 1025-1027, 1992.
18. Canan S, Ankarali S, Marangoz C. Detailed spectral profile analysis of penicillin-induced epileptiform activity in anesthetized rats. Epilepsy Res 82: 7-14, 2008.
19. Chauvette S, Volgushev M, Timofeev I. Origin of active states in local neocortical networks during slow sleep oscillation. Cereb Cortex 20: 2660-2674, 2010.
20. Chrobak JJ, Buzsáki G. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16: 3056-3066, 1996.
21. Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsáki G. Fast network oscillations in the hippocampal CA1 region of the behaving rat. J Neurosci 19: RC20, 1999.
22. Dugladze T, Vida I, Tort AB, Gross A, Otahal J, Heinemann U, Kopell NJ, Gloveli T. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc Natl Acad Sci USA 104: 17530-17535, 2007.
23. Dzhala VI, Staley KJ. Mechanisms of fast ripples in the hippocampus. J Neurosci 24: 8896-8906, 2004.
24. Filatov G, Krishnan GP, Rulkov NF, Bazhenov M. Dynamics of epileptiform activity in mouse hippocampal slices. J Biol Phys 37: 347-360, 2011.
25. Foffani G, Uzcategui YG, Gal B, Menendez de la Prida L. Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 55: 930-941, 2007.
26. Fröhlich F, Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Slow state transitions of sustained neural oscillations by activity-dependent modulation of intrinsic excitability. J Neurosci 26: 6153-6162, 2006.
27. Fröhlich F, Sejnowski TJ, Bazhenov M. Network bistability mediates spontaneous transitions between normal and pathological brain states. J Neurosci 30: 10734-10743, 2010.
28. Fröhlich F, McCormick DA. Endogenous electric fields may guide neocortical network activity. Neuron 67: 129-143, 2010.
29. Grenier F, Timofeev I, Steriade M. Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. J Neurophysiol 86: 1884-1898, 2001.
30. Heinemann U, Lux HD, Gutnick MJ. Extracellular free calcium and potassium during paroxysmal activity in the cerebral cortex of the cat. Exp Brain Res 27: 237-243, 1977.
31. Hotson JR, Prince DA. Penicillin-and barium-induced epileptiform bursting in hippocampal neurons: actions on Ca and K potentials. Ann Neurol 10: 11-17, 1981.
32. Ibarz JM, Foffani G, Cid E, Inostroza M, Menendez de la Prida L. Emergent dynamics of fast ripples in the epileptic hippocampus. J Neurosci 30: 16249-16261, 2010.
33. Izhikevich EM. Synchronization of elliptic bursters. SIAM Rev 43: 315-344, 2001.
34. Jefferys JG, Haas HL. Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission. Nature 300: 448-450, 1982.
35. Kandel A, Buzsáki G. Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat. J Neurosci 17: 6783-6797, 1997.
36. Krishnan GP, Bazhenov M. Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J Neurosci 31, 8870-8882, 2011.
37. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. Measuring phase synchrony in brain signals. Hum Brain Mapp 8: 194-208, 1999.
38. Lerma J, Herreras O, Muoz D, Sols JM. Interactions between hippocampal penicillin spikes and theta rhythm. Electroencephalogr Clin Neurophysiol 57: 532-540, 1984.
39. Lewis DV, Schuette WH. NADH fluorescence and [K ]o changes during hippocampal electrical stimulation. J Neurophysiol 38: 405-417, 1975.
40. Li X, Polygiannakis J, Kapiris P, Peratzakis A, Eftaxias K, Yao X. Fractal spectral analysis of pre-epileptic seizures in terms of criticality. J Neural Eng 2: 11-16, 2005.
41. Llinas RR, Grace AA, Yarom Y. In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10-to 50-Hz frequency range. Proc Natl Acad Sci USA 88: 897-901, 1991.
42. Lytton WW, Sejnowski TJ. Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol 66: 1059-1079, 1991.
43. Mainen ZF, Sejnowski TJ. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382: 363-366, 1996.
44. Matsumoto H, Marsan CA. cortical cellular phenomena in experimental epilepsy: interictal manifestations. Exp Neurol 9: 286-304, 1964.
45. Mitzdorf U, Singer W. Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): a current source density analysis of electrically evoked potentials. Exp Brain Res 33: 371-394, 1978.
46. Netoff TI, Schiff SJ. Decreased neuronal synchronization during experimental seizures. J Neurosci 22: 7297-7307, 2002.
47. Prince DA. The depolarization shift in "epileptic" neurons. Exp Neurol 21: 467-485, 1968a.
48. Prince DA. Inhibition in "epileptic" neurons. Exp Neurol 21: 307-321, 1968b.
49. Ray S, Maunsell JH. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol 9: e1000610, 2011.
50. Schindler K, Leung H, Elger CE, Lehnertz K. Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. Brain 130: 65-77, 2007.
51. Seigneur J, Timofeev I. Synaptic impairment induced by paroxysmal ionic conditions in neocortex. Epilepsia 52: 132-139, 2011.
52. Sirota A, Csicsvari J, Buhl D, Buzsáki G. Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA 100: 2065-2069, 2003.
53. Somers D, Kopell N. Rapid synchronization through fast threshold modulation. Biol Cybern 68: 393-407, 1993.
54. Staba RJ, Bergmann PC, Barth DS. Dissociation of slow waves and fast oscillations above 200 Hz during GABA application in rat somatosensory cortex. J Physiol 561: 205-214, 2004.
55. Staba RJ, Brett-Green B, Paulsen M, Barth DS. Effects of ventrobasal lesion and cortical cooling on fast oscillations (200 Hz) in rat somatosensory cortex. J Neurophysiol 89: 2380-2388, 2003.
56. Stasheff SF, Bragdon AC, Wilson WA. Induction of epileptiform activity in hippocampal slices by trains of electrical stimuli. Brain Res 344, 296-302, 1985.
57. Steriade M, Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37: 563-576, 2003.
58. Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsáki G. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci 31: 8605-8616, 2011.
59. Takeshita D, Bahar S. Synchronization analysis of voltage-sensitive dye imaging during focal seizures in the rat neocortex. Chaos 21: 047506, 2011.
60. Thimm J, Mechler A, Lin H, Rhee S, Lal R. Calcium-dependent open/closed conformations and interfacial energy maps of reconstituted hemichannels. J Biol Chem 280: 10646-10654, 2005.
61. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10: 1185-1199, 2000.
62. Timofeev I, Steriade M. Neocortical seizures: initiation, development and cessation. Neuroscience 123: 299-336, 2004.
63. Timofeev I, Bazhenov M, Sejnowski T, Steriade M. Cortical hyperpolarization-activated depolarizing current takes part in the generation of focal paroxysmal activities. Proc Natl Acad Sci USA 99: 9533-9537, 2002.
64. Timofeev I, Bazhenov M. Mechanisms and biological role of thalamocortical oscillations. In: Trends in Chronobiology Research, edited by Columbus F. New York: Nova Science, 2005, p. 1-47.
65. Timofeev I, Bazhenov M, Seigneur J, Sejnowski T. Neuronal synchronization and thalamocortical rhythms in sleep, wake and epilepsy. In: Jasper's Basic Mechanisms of the Epilepsies (4th ed.), edited by Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV. Bethesda, MD: National Center for Biotechnology Information, 2012.
66. Timofeeva OA, Gordon CJ. Changes in EEG power spectra and behavioral states in rats exposed to the acetylcholinesterase inhibitor chlorpyrifos and muscarinic agonist oxotremorine. Brain Res 893: 165-177, 2001.
67. Traynelis SF, Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 59: 259-276, 1988.
68. Truccolo W, Donoghue JA, Hochberg LR, Eskandar EN, Madsen JR, Anderson WS, Brown EN, Halgren E, Cash SS. Single-neuron dynamics in human focal epilepsy. Nat Neurosci 14: 635-641, 2011.
69. Wendling F, Bartolomei F, Bellanger JJ, Bourien J, Chauvel P. Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. Brain 126: 1449-1459, 2003.
70. Wong RK, Prince DA. Dendritic mechanisms underlying penicillin-induced epileptiform activity. Science 204: 1228-1231, 1979.
71. Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med 5: 557-566, 2011.
72. Ylinen A, Bragin A, Ndasdy Z, Jand G, Szab I, Sik A, Buzski G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30-46, 1995.