High-frequency oscillations and other electrophysiological biomarkers of epilepsy: Underlying mechanisms

Biomarkers in Medicine

Volumn 5, Issue 5, 2011, Pages 545-556

  Staba, Richard J ^a   Bragin, Anatol ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

epileptogenesis; epileptogenicity; fast ripple; interictal electroencephalographic spike; ripple; Upspike

Indexed keywords

BIOLOGICAL MARKER;

BRAIN ELECTROPHYSIOLOGY; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; HIGH FREQUENCY OSCILLATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HUMAN; INTERNEURON; NEOCORTEX; NONHUMAN; PYRAMIDAL NERVE CELL; REVIEW; SPIKE; SYNAPSE;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY; HIPPOCAMPUS; HUMANS;

MAMMALIA;

EID: 80054822333     PISSN: 17520363     EISSN: 17520371     Source Type: Journal    
DOI: 10.2217/bmm.11.72     Document Type: Review

References (124)

1. Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science 256, 1025-1027 (1992).
2. Chrobak JJ, Buzsaki G. High-frequency oscillations in the output of the hippocampal- entorhinal axis of the freely behaving rat. J. Neurosci. 16(9), 3056-3066 (1996).
3. Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 19(1), 274-287 (1999). (Pubitemid 29028968)
4. Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsaki G. High-frequency oscillations in human brain. Hippocampus 9, 137-142 (1999). (Pubitemid 29196957)
5. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G. Selective impairment of hippocampal g oscillations in connexin-36 knock-out mouse in vivo. J. Neurosci. 23(3), 1013-1018 (2003). (Pubitemid 36206193)
6. Staba RJ, Wilson CL, Bragin A, Jhung D, Fried I, Engel J. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann. Neurol. 56, 108-115 (2004). (Pubitemid 38857365)
7. Ulanovsky N, Moss CF. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10(2), 224-233 (2007). (Pubitemid 46174847)
8. Buzsaki G. Hippocampal sharp waves: their origin and significance. Brain Res. 398, 242-252 (1986). (Pubitemid 17210167)
9. Klausberger T, Marton LF, ONeill J, et al. Complementary roles of cholecystokinin-and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J. Neurosci. 25(42), 9782-9793 (2005). (Pubitemid 41510918)
10. Somogyi P, Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 562(Pt 1), 9-26 (2005). (Pubitemid 40207780)
11. Ylinen A, Bragin A, Nadasdy Z, et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15(1), 30-46 (1995).
12. Buzsaki G. The hippocampo-neortical dialogue. Cereb. Cortex 6, 81-92 (1996).
13. Siapas AG, Wilson MA. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 1123-1128 (1998). (Pubitemid 29018081)
14. Wierzynski CM, Lubenov EV, Gu M, Siapas AG. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61(4), 587-596 (2009).
15. Grenier F, Timofeev I, Steriade M. Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. J. Neurophysiol. 86(4), 1884-1898 (2001). (Pubitemid 32953236)
16. Kandel A, Buzsaki G. Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat. J. Neurosci. 17(17), 6783-6797 (1997). (Pubitemid 27366629)
17. Jones MS, Barth DS. Spatiotemporal organization of fast (<200 Hz) electrical oscillations in rat Vibrissa/Barrel cortex. J. Neurophysiol. 82(3), 1599-1609 (1999). (Pubitemid 29439721)
18. 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). (Pubitemid 36570202)
19. Staba RJ, Bergmann PC, Barth DS. Dissociation of slow waves and fast oscillations above 200 Hz during GABA application in rodent somatosensory cortex. J. Physiol. 561(Pt 1), 205-214 (2004). (Pubitemid 39549477)
20. Curio G, Mackert BM, Burghoff M, Koetitz R, Abraham-Fuchs K, Harer W. Localization of evoked neuromagnetic 600 Hz activity in the cerebral somatosensory system. Electroencephalogr. Clin. Neurophysiol. 91(6), 483-487 (1994).
21. Gobbele R, Waberski TD, Simon H, et al. Different origins of low- and high-frequency components (600 Hz) of human somatosensory evoked potentials. Clin. Neurophysiol. 115(4), 927-937 (2004). (Pubitemid 38293491)
22. Barth DS. Submillisecond synchronization of fast electrical oscillations in neocortex. J. Neurosci. 23(6), 2502-2510 (2003).
23. Staba RJ, Ard TD, Benison AM, Barth DS. Intracortical pathways mediate nonlinear fast oscillation (<200 Hz) interaction in rat barrel cortex. J. Neurophysiol. 93(5), 2934-2939 (2004). (Pubitemid 40570870)
24. Jones MS, MacDonald KD, Choi B, Dudek FE, Barth DS. Intracellular correlates of fast (<200 Hz) electrical oscillations in rat somatosensory cortex. J. Neurophysiol. 84, 1505-1518 (2000).
25. 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(2), 127-137 (1999). (Pubitemid 29066295)
26. Bragin A, Wilson CL, Almajano J, Mody I, Engel J Jr. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 45(9), 1017-1023 (2004). (Pubitemid 39238110)
27. Engel J Jr, Bragin A, Staba RJ, Mody I. High-frequency oscillations: what is normal and what is not? Epilepsia 50(4), 598-604 (2009).
28. Staba RJ, Wilson CL, Bragin A, Fried I, Engel J Jr. Quantitative analysis of high frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol. 88, 1743-1752 (2002). (Pubitemid 35191178)
29. Bragin A, Wilson CL, Staba RJ, Reddick M, Fried I, Engel J Jr. Interictal high frequency oscillations (80-500 Hz) in the human epileptic brain: entorhinal cortex. Ann. Neurol. 52(4), 407-415 (2002).
30. Staba RJ, Frighetto L, Behnke EJ, et al. Increased fast ripple to ripple ratios correlate with reduced hippocampal volumes and neuron loss in temporal lobe epilepsy patients. Epilepsia 48(11), 2130-2138 (2007). (Pubitemid 350098762)
31. Jacobs J, Levan P, Chatillon CE, Olivier A, Dubeau F, Gotman J. High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. Brain 132(Pt 4), 1022-1037 (2009).
32. Le Van Quyen M, Bragin A, Staba R, Crepon B, Wilson CL, Engel J Jr. Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J. Neurosci. 28(24), 6104-6110 (2008).
33. Clemens Z, Molle M, Eross L, Barsi P, Halasz P, Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130(11), 2868-2878 (2007). (Pubitemid 350041476)
34. Nir Y, Staba RJ, Andrillon T, et al. Regional slow waves and spindles in human sleep. Neuron 70(1), 153-169 (2011).
35. Grenier F, Timofeev I, Steriade M. Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates. J. Neurophysiol. 89(2), 841-852 (2003). (Pubitemid 36206133)
36. Bragin A, Mody I, Wilson CL, Engel J Jr. Local generation of fast ripples in epileptic brain. J. Neurosci. 22(5), 2012-2021 (2002). (Pubitemid 35386321)
37. Bragin A, Wilson CL, Engel J Jr. Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41(Suppl. 6), S144-S152 (2000).
38. Bragin A, Wilson CL, Engel J Jr. Voltage depth profiles of high-frequency oscillations after kainic acid-induced status epilepticus. Epilepsia 48(Suppl. 5), 35-40 (2007). (Pubitemid 47512200)
39. Bragin A, Benassi SK, Kheiri F, Engel J Jr. Further evidence that pathologic high-frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus. Epilepsia 52(1), 45-52 (2011).
40. Dzhala VI, Staley KJ. Mechanisms of fast ripples in the hippocampus. J. Neurosci. 24(40), 8896-8906 (2004). (Pubitemid 39362985)
41. 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(6), 930-941 (2007). (Pubitemid 47391186)
42. 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(48), 16249-16261 (2010).
43. Jefferys JG. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol. Rev. 75(4), 689-723 (1995).
44. Jiruska P, Powell AD, Chang WC, Jefferys JG. Electrographic high-frequency activity and epilepsy. Epilepsy Res. 89(1), 60-65 (2010).
45. Ko¨hling R, Staley K. Network mechanisms for fast ripple activity in epileptic tissue. Epilepsy Res. DOI: 10.1016/j. eplepsyres.2011.03.006 (2011) (Epub ahead of print).
46. Draguhn A, Traub RD, Schmitz D, Jefferys JGR. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189-192 (1998). (Pubitemid 28325973)
47. Jiruska P, Csicsvari J, Powell AD, et al. High-frequency network activity, global increase in neuronal activity, and synchrony expansion precede epileptic seizures in vitro. J. Neurosci. 30(16), 5690-5701 (2010).
48. Traub RD, Schmitz D, Jefferys JG, Draguhn A. High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions. Neuroscience 92(2), 407-426 (1999). (Pubitemid 29268033)
49. Traub RD, Whittington MA, Buhl EH, et al. A possible role for gap junctions in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia 42(2), 153-170 (2001). (Pubitemid 32204795)
50. Bragin A, Wilson CL, Engel JJ. Spatial stability over time of brain areas generating fast ripples in the epileptic rat. Epilepsia 44(9), 1233-1237 (2003). (Pubitemid 37100050)
51. Jacobs J, Zijlmans M, Zelmann R, et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann. Neurol. 67(2), 209-220 (2010).
52. Wu JY, Sankar R, Lerner JT, Matsumoto JH, Vinters HV, Mathern GW. Removing interictal fast ripples on electrocorticography linked with seizure freedom in children. Neurology 75(19), 1686-1694 (2010).
53. Ogren JA, Wilson CL, Bragin A, et al. Three dimensional surface maps link local atrophy and fast ripples in human epileptic hippocampus. Ann. Neurol. 66(6), 783-791 (2009).
54. Van Gompel JJ, Stead SM, Giannini C, et al. Phase I trial: safety and feasibility of intracranial electroencephalography using hybrid subdural electrodes containing macro- and microelectrode arrays. Neurosurg. Focus 25(3), E23 (2008).
55. Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomarkers Med. 5(5), 557-566 (2011).
56. Urrestarazu E, Chander R, Dubeau F, Gotman J. Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain 130(9), 2354-2366 (2007). (Pubitemid 47327627)
57. Jacobs J, LeVan P, Chander R, Hall J, Dubeau F, Gotman J. Interictal high-frequency oscillations (80-500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia 49(11), 1893-1907 (2008).
58. Worrell GA, Gardner AB, Stead SM, et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain 131(4), 928-937 (2008). (Pubitemid 351499420)
59. Schevon CA, Trevelyan AJ, Schroeder CE, Goodman RR, McKhann G Jr, Emerson RG. Spatial characterization of interictal high frequency oscillations in epileptic neocortex. Brain 132(11), 3047-3059 (2009).
60. A glossary of terms most commonly used by clinical electroencephalographers. Electroencephalogr. Clin. Neurophysiol. 37(5), 538-548 (1974).
61. de Curtis M, Avanzini G. Interictal spikes in focal epileptogenesis. Prog. Neurobiol. 63, 541-567 (2001). (Pubitemid 32115432)
62. Matsumoto H, Marsan CA. Cortical cellular phenomena in experimental epilepsy: interictal manifestations. Exp. Neurol. 9, 286-304 (1964).
63. Dichter M, Spencer WA. Penicillin-induced interictal discharges from the cat hippocampus. I. Characteristics and topographical features. J. Neurophysiol. 32, 649-662 (1969).
64. Prince DA, Futamachi KJ. Intracellular recordings from chronic epileptogenic foci in the monkey. Electroencephalogr. Clin. Neurophysiol. 29(5), 496-510 (1970).
65. Mody I, Lambert JD, Heinemann U. Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J. Neurophysiol. 57(3), 869-888 (1987). (Pubitemid 17047666)
66. Haas HL, Jefferys JG. Low-calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. J. Physiol. 354, 185-201 (1984). (Pubitemid 14066362)
67. Rutecki PA, Lebeda FJ, Johnston D. Epileptiform activity induced by changes in extracellular potassium in hippocampus. J. Neurophysiol. 54(5), 1363-1374 (1985). (Pubitemid 16210121)
68. Ben-Ari Y, Tremblay E, Ottersen OP. Injections of kainic acid into the amygdaloid complex of the rat: an electrographic, clinical and histological study in relation to the pathology of epilepsy. Neuroscience 5(3), 515-528 (1980). (Pubitemid 10131222)
69. Lothman EW, Bertram EH, Bekenstein JW, Perlin JB. Self-sustaining limbic status epilepticus induced by continuous hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res. 3(2), 107-119 (1989). (Pubitemid 19071179)
70. Prince DA, Wong RK. Human epileptic neurons studied in vitro. Brain Res. 210(1-2), 323-333 (1981). (Pubitemid 11145579)
71. Schwartzkroin PA, Haglund MM. Spontaneous rhythmic synchronous activity in epileptic human and normal monkey temporal lobe. Epilepsia 27(5), 523-533 (1986). (Pubitemid 16026047)
72. Hwa GG, Avoli M, Oliver A, Villemure JG. Bicuculline-induced epileptogenesis in the human neocortex maintained in vitro. Exp. Brain Res. 83(2), 329-339 (1991).
73. Schwartzkroin PA, Prince DA. Effects of TEA on hippocampal neurons. Brain Res. 185(1), 169-181 (1980). (Pubitemid 10144873)
74. Prince DA. The depolarization shift in epileptic neurons. Exp. Neurol. 21(4), 467-185 (1968).
75. Matsumoto H, Ayala GF, Gumnit RJ. Neuronal behavior and triggering mechanism in cortical epileptic focus. J. Neurophysiol. 32(5), 688-703 (1969).
76. Dichter M, Spencer WA. Penicillin-induced interictal discharges from the cat hippocampus. II. Mechanisms underlying origin and restriction. J. Neurophysiol. 32(5), 663-687 (1969).
77. Johnston D, Brown TH. Giant synaptic potential hypothesis for epileptiform activity. Science 211(4479), 294-297 (1981). (Pubitemid 11131079)
78. Johnston D, Brown TH. The synaptic nature of the paroxysmal depolarizing shift in hippocampal neurons. Ann. Neurol. 16(Suppl.), S65-S71 (1984). (Pubitemid 15202055)
79. Dichter MA, Ayala GF. Cellular mechanisms of epilepsy: a status report. Science 237(4811), 157-164 (1987). (Pubitemid 17095917)
80. Schwartzkroin PA. Characteristics of CA1 neurons recorded intracellularly in the hippocampal in vitro slice preparation. Brain Res. 85(3), 423-436 (1975).
81. Wong RK, Prince DA. Participation of calcium spikes during intrinsic burst firing in hippocampal neurons. Brain Res. 159(2), 385-390 (1978). (Pubitemid 9033716)
82. Connors BW, Gutnick MJ, Prince DA. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48(6), 1302-1320 (1982). (Pubitemid 13224459)
83. Stafstrom CE, Schwindt PC, Chubb MC, Crill WE. Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 53(1), 153-170 (1985). (Pubitemid 15174281)
84. Azouz R, Jensen MS, Yaari Y. Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. 492(Pt 1), 211-223 (1996). (Pubitemid 26123645)
85. Chen S, Su H, Yue C, et al. An increase in persistent sodium current contributes to intrinsic neuronal bursting after status epilepticus. J. Neurophysiol. 105(1), 117-129 (2011).
86. Sanabria ER, Su H, Yaari Y. Initiation of network bursts by Ca2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J. Physiol. 532(Pt 1), 205-216 (2001). (Pubitemid 32303283)
87. Su H, Sochivko D, Becker A, et al. Upregulation of a T-type Ca2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J. Neurosci. 22(9), 3645-3655 (2002). (Pubitemid 37465769)
88. Kang N, Xu J, Xu Q, Nedergaard M, Kang J. Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 94(6), 4121-4130 (2005). (Pubitemid 41691773)
89. MacVicar BA, Dudek FE. Local synaptic circuits in rat hippocampus: interactions between pyramidal cells. Brain Res. 184(1), 220-223 (1980). (Pubitemid 10128413)
90. Traub RD, Wong RK. Cellular mechanism of neuronal synchronization in epilepsy. Science 216(4547), 745-747 (1982). (Pubitemid 12121256)
91. Miles R, Wong RKS. Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306, 371-373 (1983). (Pubitemid 14242746)
92. Jefferys JG, Haas HL. Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission. Nature 300(5891), 448-450 (1982). (Pubitemid 13182910)
93. Taylor CP, Dudek FE. Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 218(4574), 810-812 (1982). (Pubitemid 13251523)
94. MacVicar BA, Dudek FE. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213(4509), 782-785 (1981). (Pubitemid 11016461)
95. Schmitz D, Schuchmann S, Fisahn A, et al. Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31(5), 831-840 (2001). (Pubitemid 32907377)
96. Nadler JV. The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res. 28(11), 1649-1658 (2003). (Pubitemid 37296207)
97. Sloviter RS, Zappone CA, Harvey BD, Frotscher M. Kainic acid-induced recurrent mossy fiber innervation of dentate gyrus inhibitory interneurons: possible anatomical substrate of granule cell hyper-inhibition in chronically epileptic rats. J. Comp. Neurol. 494(6), 944-960 (2006). (Pubitemid 43063988)
98. Wilson CL, Khan SU, Engel J Jr, Isokawa M, Babb TL, Behnke EJ. Paired pulse suppression and facilitation in human epileptogenic hippocampal formation. Epilepsy Res. 31, 211-230 (1998). (Pubitemid 28370847)
99. Isokawα-Akesson M, Wilson CL, Babb TL. Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res. 3, 236-247 (1989). (Pubitemid 19131413)
100. Gregory RP, Oates T, Merry RT. Electroencephalogram epileptiform abnormalities in candidates for aircrew training. Electroencephalogr. Clin. Neurophysiol. 86(1), 75-77 (1993). (Pubitemid 23023927)
101. Okubo Y, Matsuura M, Asai T, et al. A follow-up study of healthy children with epileptiform EEG discharges. J. Epilepsy 6(4), 250-256 (1993).
102. Sam MC, So EL. Significance of epileptiform discharges in patients without epilepsy in the community. Epilepsia 42(10), 1273-1278 (2001). (Pubitemid 33070667)
103. Gotman J, Marciani MG. Electroencephalographic spiking activity, drug levels, and seizure occurrence in epileptic patients. Ann. Neurol. 17(6), 597-603 (1985). (Pubitemid 15055579)
104. Gotman J. Relationships between interictal spiking and seizures: human and experimental evidence. Can. J. Neurol. Sci. 18(4 Suppl.), 573-576 (1991).
105. Barbarosie M, Louvel J, Kurcewicz I, Avoli M. CA3-released entorhinal seizures disclose dentate gyrus epileptogenicity and unmask a temporoammonic pathway. J. Neurophysiol. 83(3), 1115-1124 (2000). (Pubitemid 30159543)
106. Engel J Jr, Ackermann RF. Interictal EEG spikes correlate with decreased, rather than increased, epileptogenicity in amygdaloid kindled rats. Brain Res. 190(2), 543-548 (1980). (Pubitemid 10085058)
107. Librizzi L, de Curtis M. Epileptiform ictal discharges are prevented by periodic interictal spiking in the olfactory cortex. Ann. Neurol. 53(3), 382-389 (2003). (Pubitemid 36258642)
108. Avoli M, Biagini G, de Curtis M. Do interictal spikes sustain seizures and epileptogenesis? Epilepsy Curr. 6(6), 203-207 (2006).
109. Urrestarazu E, Jirsch JD, Le Van P, et al. High-frequency intracerebral EEG activity (100-500 Hz) following interictal spikes. Epilepsia 47(9), 1465-1476 (2006). (Pubitemid 44393859)
110. Bragin A, Engel J Jr, Staba RJ. High-frequency oscillations in epileptic brain. Curr. Opin. Neurol. 23(2), 151-156 (2010).
111. Staley K, Hellier JL, Dudek FE. Do interictal spikes drive epileptogenesis? Neuroscientist 11(4), 272-276 (2005). (Pubitemid 41043227)
112. Staley KJ, Dudek FE. Interictal spikes and epileptogenesis. Epilepsy Curr. 6(6), 199-202 (2006).
113. Hellier JL, Patrylo PR, Dou P, Nett M, Rose GM, Dudek FE. Assessment of inhibition and epileptiform activity in the septal dentate gyrus of freely behaving rats during the first week after kainate treatment. J. Neurosci. 19(22), 10053-10064 (1999). (Pubitemid 30226677)
114. White A, Williams PA, Hellier JL, Clark S, Edward Dudek F, Staley KJ. EEG spike activity precedes epilepsy after kainate-induced status epilepticus. Epilepsia 51(3), 371-383 (2010).
115. Toth Z, Hollrigel GS, Gorcs T, Soltesz I. Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J. Neurosci. 17(21), 8106-8117 (1997). (Pubitemid 27461035)
116. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679-685 (1993). (Pubitemid 23350685)
117. Steriade M, Contreras D, Curro Dossi R, Nunez A. The slow). (Pubitemid 23241168)
118. Amzica F, Steriade M. Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. J. Neurosci. 15(6), 4658-4677 (1995).
119. Tononi G, Cirelli C. Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull. 62(2), 143-150 (2003). (Pubitemid 37443660)
120. Knutson KL. Impact of sleep and sleep loss on glucose homeostasis and appetite regulation. Sleep Med. Clin. 2(2), 187-197 (2007).
121. He de F, Ma DL, Tang YC, Engel J Jr, Bragin A, Tang FR. Morpho-physiologic characteristics of dorsal subicular network in mice after pilocarpine-induced status epilepticus. Brain Pathol. 20(1), 80-95 (2010).
122. Kobayashi K, Watanabe Y, Inoue T, Oka M, Yoshinaga H, Ohtsuka Y. Scalp-recorded high-frequency oscillations in childhood sleep-induced electrical status epilepticus. Epilepsia 51(10), 2190-2194 (2010).
123. Andrade-Valenca LP, Dubeau F, Mari F, Zelmann R, Gotman J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology 77(6), 524-531 (2011).
124. Kobayashi K, Yoshinaga H, Toda Y, Inoue T, Oka M, Ohtsuka Y. High-frequency oscillations in idiopathic partial epilepsy of childhood. Epilepsia DOI: 10.1111/j.1528-1167.2011.03169.x (2011) (Epub ahead of print).