SpringerLink
Log in

Electrophysiological Biomarkers of Epilepsy

  • Review
  • Published:
Neurotherapeutics

Abstract

In patients being evaluated for epilepsy and in animal models of epilepsy, electrophysiological recordings are carried to capture seizures to determine the existence of epilepsy. Electroencephalography recordings from the scalp, or sometimes directly from the brain, are also used to locate brain areas where seizure begins, and in surgical treatment help plan the area for resection. As seizures are unpredictable and can occur infrequently, ictal recordings are not ideal in terms of time, cost, or risk when, for example, determining the efficacy of existing or new anti-seizure drugs, evaluating potential anti-epileptogenic interventions, or for prolonged intracerebral electrode studies. Thus, there is a need to identify and validate other electrophysiological biomarkers of epilepsy that could be used to diagnose, treat, cure, and prevent epilepsy. Electroencephalography recordings in the epileptic brain contain other interictal electrophysiological disturbances that can occur more frequently than seizures, such as interictal spikes (IIS) and sharp waves, and from invasive studies using wide bandwidth recording and small diameter electrodes, the discovery of pathological high-frequency oscillations (HFOs) and microseizures. Of IIS, HFOs, and microseizures, a significant amount of recent research has focused on HFOs in the pathophysiology of epilepsy. Results from studies in animals with epilepsy and presurgical patients have consistently found a strong association between HFOs and epileptogenic brain tissue that suggest HFOs could be a potential biomarker of epileptogenicity and epileptogenesis. Here, we discuss several aspects of HFOs, as well as IIS and microseizures, and the evidence that supports their role as biomarkers of epilepsy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Pitkanen A. Therapeutic approaches to epileptogenesis—hope on the horizon. Epilepsia 2010;51(Suppl. 3):2-17.

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Engel J, Jr., Pitkanen A, Loeb JA, et al. Epilepsy biomarkers. Epilepsia 2013;54(Suppl. 4):61-69.

    PubMed  Google Scholar 

  3. Bragin A, Engel J, Jr., Wilson CL, et al. High-frequency oscillations in human brain. Hippocampus 1999;9:137-142.

    CAS  PubMed  Google Scholar 

  4. Bragin A, Engel J, Jr., Wilson CL, et al. Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 1999;40:127-137.

    CAS  PubMed  Google Scholar 

  5. Stead M, Bower M, Brinkmann BH, et al. Microseizures and the spatiotemporal scales of human partial epilepsy. Brain 2010;133:2789-2797.

    PubMed Central  PubMed  Google Scholar 

  6. Schevon CA, Goodman RR, McKhann G, Jr., Emerson RG. Propagation of epileptiform activity on a submillimeter scale. J Clin Neurophysiol 2010;27:406-411.

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Vanhatalo S, Voipio J, Kaila K. Full-band EEG (FbEEG): an emerging standard in electroencephalography. Clin Neurophysiol 2005;116:1-8.

    PubMed  Google Scholar 

  8. Worrell GA, Jerbi K, Kobayashi K, et al. Recording and analysis techniques for high-frequency oscillations. Prog Neurobiol 2012;98:265-278.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Wirrell EC. Prognostic significance of interictal epileptiform discharges in newly diagnosed seizure disorders. J Clin Neurophysiol 2010;27:239-248.

    PubMed  Google Scholar 

  10. So EL. Interictal epileptiform discharges in persons without a history of seizures: what do they mean? J Clin Neurophysiol 2010;27:229-238.

    PubMed  Google Scholar 

  11. Gotman J, Marciani MG. Electroencephalographic spiking activity, drug levels, and seizure occurrence in epileptic patients. Ann Neurol 1985;17:597-603.

    CAS  PubMed  Google Scholar 

  12. Gotman J, Koffler DJ. Interictal spiking increases after seizures but does not after decrease in medication. Electroencephalogr Clin Neurophysiol 1989;72:7-15.

    CAS  PubMed  Google Scholar 

  13. Spencer SS, Goncharova, II, Duckrow RB, et al. Interictal spikes on intracranial recording: behavior, physiology, and implications. Epilepsia 2008;49:1881-1892.

    PubMed  Google Scholar 

  14. Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med 2011;5:557-566.

    PubMed Central  PubMed  Google Scholar 

  15. Steinhoff BJ, Scholly J, Dentel C, Staack AM. Is routine electroencephalography (EEG) a useful biomarker for pharmacoresistant epilepsy? Epilepsia 2013;54(Suppl. 2):63-66.

    CAS  PubMed  Google Scholar 

  16. White A, Williams PA, Hellier JL, et al. EEG spike activity precedes epilepsy after kainate-induced status epilepticus. Epilepsia 2010;51:371-383.

    PubMed Central  PubMed  Google Scholar 

  17. Chauviere L, Doublet T, Ghestem A, et al. Changes in interictal spike features precede the onset of temporal lobe epilepsy. Ann Neurol 2012;71:805-814.

    PubMed  Google Scholar 

  18. Huneau C, Benquet P, Dieuset G, et al. Shape features of epileptic spikes are a marker of epileptogenesis in mice. Epilepsia 2013;54:2219-2227.

    PubMed  Google Scholar 

  19. Staley KJ, White A, Dudek FE. Interictal spikes: Harbingers or causes of epilepsy? Neurosci Lett 2011;497:247-250.

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Avoli M, de Curtis M, Kohling R. Does interictal synchronization influence ictogenesis? Neuropharmacology 2013;69:37-44.

    CAS  PubMed  Google Scholar 

  21. Staba RJ, Bragin A. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: underlying mechanisms. Biomark Med 2011;5:545-556.

    PubMed Central  PubMed  Google Scholar 

  22. Jacobs J, Staba R, Asano E, et al. High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol 2012;98:302-315.

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Engel J, Jr., da Silva FL. High-frequency oscillations - where we are and where we need to go. Prog Neurobiol 2012;98:316-318.

    PubMed Central  PubMed  Google Scholar 

  24. Engel J, Jr. , Bragin A, Staba RJ, Mody I. High-frequency oscillations: What is normal and what is not? Epilepsia 2009;50:598-604.

    PubMed  Google Scholar 

  25. Matsumoto A, Brinkmann BH, Stead SM, et al. Pathological and physiological high frequency oscillations in focal human epilepsy. J Neurophysiol 2013;110:1958-1964.

    PubMed  Google Scholar 

  26. Gloss D, Nolan SJ, Staba R. The role of high-frequency oscillations in epilepsy surgery planning . Cochrane Database Syst Rev 2014, Issue 1. Art. No.: CD010235. doi:10.1002/14651858.CD010235.pub2

  27. Jefferys JG, de la Prida LM, Wendling F, et al. Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol 2012;98:250-64.

    PubMed  Google Scholar 

  28. Grenier F, Timofeev I, Steriade M. Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. J Neurophysiol 2001;86:1884-1898.

    CAS  PubMed  Google Scholar 

  29. Staba RJ, Wilson CL, Bragin A, et al. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann Neurol 2004;56:108-115.

    PubMed  Google Scholar 

  30. Bagshaw AP, Jacobs J, LeVan P, et al. Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy. Epilepsia 2008;50:617-628.

    Google Scholar 

  31. Bragin A, Engel J, Jr., Staba RJ. High-frequency oscillations in epileptic brain. Curr Opin Neurol 2010;23:151-156.

    PubMed  Google Scholar 

  32. Menendez de la Prida L, Trevelyan AJ. Cellular mechanisms of high frequency oscillations in epilepsy: On the diverse sources of pathological activities. Epilepsy Res 2011;97:308-317.

    PubMed  Google Scholar 

  33. Staba RJ. Normal and pathologic high-frequency oscillations. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV (eds) Jasper’s basic mechanisms of the epilepsies. 4th ed. Bethesda, MD. Oxford University Press, Inc. 2012;202-212.

  34. Buzsaki G, Horvath Z, Urioste R, et al. High-frequency network oscillation in the hippocampus. Science 1992;256:1025-1027.

    CAS  PubMed  Google Scholar 

  35. Jones MS, Barth DS. Spatiotemporal organization of fast (>200 Hz) electrical oscillations in rat Vibrissa/Barrel cortex. J Neurophysiol 1999;82:1599-1609.

    CAS  PubMed  Google Scholar 

  36. Csicsvari J, Hirase H, Czurko A, et al. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 1999;19:274-287.

    CAS  PubMed  Google Scholar 

  37. Ylinen A, Bragin A, Nadasdy Z, et al. Sharp wave-associated high-frequency oscillation (200Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 1995;15:30-46.

    CAS  PubMed  Google Scholar 

  38. Klausberger T, Magill PJ, Marton LF, et al. Brain-state and cell-type specific firing of hippocampal interneurons in vivo. Nature 2003;42:844-848.

    Google Scholar 

  39. Jones MS, MacDonald KD, Choi B, et al. Intracellular correlates of fast (>200 Hz) electrical oscillations in rat somatosensory cortex. J Neurophysiol 2000;84:1505-1518.

    CAS  PubMed  Google Scholar 

  40. Singer W. Synchronization of Cortical activity and its putative role in information processing and learning. Annu Rev Physiol 1993;55:349-374.

    CAS  PubMed  Google Scholar 

  41. Murthy VN, Fetz EE. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci U S A 1992;89:5670-5674.

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Buzsaki G. The Hippocampo-neortical dialogue. Cereb Cortex 1996;6:81-92.

    CAS  PubMed  Google Scholar 

  43. Bragin A, Wilson CL, Engel J, Jr. Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: A hypothesis. Epilepsia 2000;41(Suppl. 6):S144-S152.

    PubMed  Google Scholar 

  44. Bragin A, Wilson CL, Engel J, Jr. Voltage depth profiles of high-frequency oscillations after kainic acid-induced status epilepticus. Epilepsia 2007;48:35-40.

    CAS  PubMed  Google Scholar 

  45. Bragin A, Wilson CL, Almajano J, et al. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 2004;45:1017-1023.

    PubMed  Google Scholar 

  46. Dzhala VI, Staley KJ. Mechanisms of fast ripples in the hippocampus. J Neurosci 2004;24:8896-8906.

    CAS  PubMed  Google Scholar 

  47. D’Antuono M, de Guzman P, Kano T, Avoli M. Ripple activity in the dentate gyrus of disinhibited hippocampus-entorhinal cortex slices. J Neurosci Res 2005;80:92-103.

    PubMed  Google Scholar 

  48. 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 2007;55:930-941.

    CAS  PubMed  Google Scholar 

  49. 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 2011;52:45-52.

    PubMed Central  PubMed  Google Scholar 

  50. Grenier F, Timofeev I, Steriade M. Neocortical very fast oscillations (ripples, 80–200 Hz) during seizures: intracellular correlates. J Neurophysiol 2003;89:841-852.

    PubMed  Google Scholar 

  51. Trevelyan AJ. The direct relationship between inhibitory currents and local field potentials. J Neurosci 2009;29:15299-15307.

    CAS  PubMed  Google Scholar 

  52. Ibarz JM, Foffani G, Cid E, et al. Emergent dynamics of fast ripples in the epileptic hippocampus. J Neurosci 2010;30:16249-16261.

    CAS  PubMed  Google Scholar 

  53. Colder BW, Wilson CL, Frysinger RC, et al. Interspike intervals during interictal periods in human temporal lobe epilepsy. Brain Res 1996;719:96-103.

    CAS  PubMed  Google Scholar 

  54. Staba RJ, Wilson CL, Fried I, Engel J, Jr. Single neuron burst firing in the human hippocampus during sleep. Hippocampus 2002;12:724-734.

    PubMed  Google Scholar 

  55. Staba RJ, Wilson CL, Bragin A, et al. Sleep states differentiate single neuron activity recorded from human epileptic hippocampus, entorhinal cortex, and subiculum. J Neurosci 2002;22:5694-5704.

    CAS  PubMed  Google Scholar 

  56. Simon A, Traub RD, Vladimirov N, et al. Gap junction networks can generate both ripple-like and fast ripple-like oscillations. Eur J Neurosci 2014;39:46-60.

    PubMed  Google Scholar 

  57. 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 2010;30:5690-5701.

    CAS  PubMed  Google Scholar 

  58. Demont-Guignard S, Benquet P, Gerber U, et al. Distinct hyperexcitability mechanisms underlie fast ripples and epileptic spikes. Ann Neurol 2012;71:342-352.

    PubMed  Google Scholar 

  59. Kohling R, Staley K. Network mechanisms for fast ripple activity in epileptic tissue. Epilepsy Res 2011;97:318-323.

    PubMed Central  PubMed  Google Scholar 

  60. Bragin A, Mody I, Wilson CL, Engel J, Jr. Local generation of fast ripples in epileptic brain. J Neurosci 2002;22:2012-2021.

    CAS  PubMed  Google Scholar 

  61. Urrestarazu E, Chander R, Dubeau F, Gotman J. Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain 2007;130:2354-2366.

    PubMed  Google Scholar 

  62. Khosravani H, Mehrotra N, Rigby M, et al. Spatial localization and time-dependant changes of electrographic high frequency oscillations in human temporal lobe epilepsy. Epilepsia 2008;50:605-616.

    PubMed  Google Scholar 

  63. Crepon B, Navarro V, Hasboun D, et al. Map** interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. Brain 2010;133:33-45.

    PubMed  Google Scholar 

  64. Akiyama T, McCoy B, Go CY, et al. Focal resection of fast ripples on extraoperative intracranial EEG improves seizure outcome in pediatric epilepsy. Epilepsia 2011;52:1802-11.

    PubMed  Google Scholar 

  65. Worrell GA, Gardner AB, Stead SM, et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain 2008;131:928-937.

    PubMed Central  PubMed  Google Scholar 

  66. Chatillon CE, Zelmann R, Bortel A, et al. Contact size does not affect high frequency oscillation detection in intracerebral EEG recordings in a rat epilepsy model. Clin Neurophysiol 2011;122:1701-1705.

    PubMed Central  PubMed  Google Scholar 

  67. Chatillon CE, Zelmann R, Hall JA, et al. Influence of contact size on the detection of HFOs in human intracerebral EEG recordings. Clin Neurophysiol 2013;124:1541-1546.

    CAS  PubMed  Google Scholar 

  68. Stacey WC, Kellis S, Greger B, et al. Potential for unreliable interpretation of EEG recorded with microelectrodes. Epilepsia 2013;54:1391-1401.

    PubMed  Google Scholar 

  69. Zelmann R, Zijlmans M, Jacobs J, et al. Improving the identification of high frequency oscillations. Clin Neurophysiol 2009;120:1457-1464.

    PubMed Central  PubMed  Google Scholar 

  70. Zijlmans M, Jacobs J, Zelmann R, et al. High-frequency oscillations mirror disease activity in patients with epilepsy. Neurology 2009;72:979-986.

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Pearce A, Wulsin D, Blanco JA, et al. Temporal changes of neocortical high-frequency oscillations in epilepsy. J Neurophysiol 2013;110:1167-1179.

    PubMed  Google Scholar 

  72. Benar CG, Chauviere L, Bartolomei F, Wendling F. Pitfalls of high-pass filtering for detecting epileptic oscillations: a technical note on “false” ripples. Clin Neurophysiol 2010;121:301-310.

    CAS  PubMed  Google Scholar 

  73. Worrell G. High-frequency oscillations recorded on scalp EEG. Epilepsy Curr 2012;12:57-58.

    PubMed Central  PubMed  Google Scholar 

  74. Staba RJ, Wilson CL, Bragin A, et al. Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 2002;88:1743-1752.

    PubMed  Google Scholar 

  75. Gardner AB, Worrell GA, Marsh E, et al. Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings. Clin Neurophysiol 2007;118:1134-1143.

    PubMed Central  PubMed  Google Scholar 

  76. Blanco JA, Stead M, Krieger A, et al. Data mining neocortical high-frequency oscillations in epilepsy and controls. Brain 2011;134:2948-2959.

    PubMed Central  PubMed  Google Scholar 

  77. Zelmann R, Mari F, Jacobs J, et al. A comparison between detectors of high frequency oscillations. Clin Neurophysiol 2012;123:106-116.

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Birot G, Kachenoura A, Albera L, et al. Automatic detection of fast ripples. J Neurosci Methods 2013;213:236-249.

    PubMed  Google Scholar 

  79. Schevon CA, Ng SK, Cappell J, et al. Microphysiology of epileptiform activity in human neocortex. J Clin Neurophysiol 2008;25:321-330.

    PubMed Central  PubMed  Google Scholar 

  80. Mountcastle VB. An organization principle for cerebral function: the unit module and the distributed system. In: Petsche H, Hughes JR (eds) The mindful brain. Cambridge, MA, MIT Press, 1978:7-50

    Google Scholar 

  81. Ebersole JS, Pedley TA. Current practice of clinical electroencephalography. Philadelphia, PA, Lippincott Williams & Wilkins, 2003.

    Google Scholar 

  82. Gray CM, Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A 1989;86:1698-1702.

    CAS  PubMed Central  PubMed  Google Scholar 

  83. Bragin A, Azizyan A, Almajano J, et al. Analysis of chronic seizure onsets after intrahippocampal kainic acid injection in freely moving rats. Epilepsia 2005;46:1592-1598.

    PubMed  Google Scholar 

  84. Levesque M, Salami P, Gotman J, Avoli M. Two seizure-onset types reveal specific patterns of high-frequency oscillations in a model of temporal lobe epilepsy. J Neurosci 2012;32:13264-13272.

    CAS  PubMed  Google Scholar 

  85. Gnatkovsky V, Librizzi L, Trombin F, de Curtis M. Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann Neurol 2008;64:674-686.

    PubMed  Google Scholar 

  86. Fisher RS, Webber WR, Lesser RP, et al. High-frequency EEG activity at the start of seizures. J Clin Neurophysiol 1992;9:441-448.

    CAS  PubMed  Google Scholar 

  87. Allen PJ, Fish DR, Smith SJ. Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. Electroencephalogr Clin Neurophysiol 1992;82:155-159.

    CAS  PubMed  Google Scholar 

  88. 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 2001;42:153-170.

    CAS  PubMed  Google Scholar 

  89. Worrell GA, Parish L, Cranstoun SD, et al. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 2004;127:1496-1506.

    PubMed  Google Scholar 

  90. Jirsch JD, Urrestarazu E, LeVan P, et al. High-frequency oscillations during human focal seizures. Brain 2006;129:1593-1608.

    CAS  PubMed  Google Scholar 

  91. Ochi A, Otsubo H, Donner EJ, et al. Dynamic changes of ictal high-frequency oscillations in neocortical epilepsy: using multiple band frequency analysis. Epilepsia 2007;48:286-296.

    PubMed  Google Scholar 

  92. Akiyama T, Otsubo H, Ochi A, et al. Focal cortical high-frequency oscillations trigger epileptic spasms: Confirmation by digital video subdural EEG. Clin Neurophysiol 2005;116:2819-2825.

    PubMed  Google Scholar 

  93. Akiyama T, Otsubo H, Ochi A, et al. Topographic Movie of ictal high-frequency oscillations on the brain surface using subdural EEG in neocortical epilepsy. Epilepsia 2006;47:1953-1957.

    PubMed  Google Scholar 

  94. RamachandranNair R, Ochi A, Imai K, et al. Epileptic spasms in older pediatric patients: MEG and ictal high-frequency oscillations suggest focal-onset seizures in a subset of epileptic spasms. Epilepsy Res 2008;78:216-224.

    PubMed  Google Scholar 

  95. Nariai H, Nagasawa T, Juhasz C, et al. Statistical map** of ictal high-frequency oscillations in epileptic spasms. Epilepsia 2011;52:63-74.

    PubMed Central  PubMed  Google Scholar 

  96. Jacobs J, Zelmann R, Jirsch J, et al. High frequency oscillations (80–500 Hz) in the preictal period in patients with focal seizures. Epilepsia 2009;50:1780-1792.

    PubMed Central  PubMed  Google Scholar 

  97. Bragin A, Wilson CL, Staba RJ, et al. Interictal high-frequency oscillations (80–500 Hz) in the human epileptic brain: entorhinal cortex. Ann Neurol 2002;52:407-415.

    PubMed  Google Scholar 

  98. 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 2007;48:2130-2138.

    PubMed  Google Scholar 

  99. Ogren JA, Wilson CL, Bragin A, et al. Three dimensional surface maps link local atrophy and fast ripples in human epileptic hippocampus. Ann Neurol 2009;66:783-791.

    PubMed Central  PubMed  Google Scholar 

  100. Urrestarazu E, Jirsch JD, Le Van P, et al. High-frequency intracerebral EEG activity (100–500 Hz) following interictal spikes. Epilepsia 2006;47:1465-1476.

    PubMed  Google Scholar 

  101. Jacobs J, LeVan P, Chander R, et al. Interictal high-frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia 2008;49:1893-1907.

    PubMed Central  PubMed  Google Scholar 

  102. Jacobs J, Levan P, Chatillon CE, et al. High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. Brain 2009;132:1022-1037.

    PubMed Central  PubMed  Google Scholar 

  103. Andrade-Valenca L, Mari F, Jacobs J, et al. Interictal high frequency oscillations (HFOs) in patients with focal epilepsy and normal MRI. Clin Neurophysiol 2012;123:100-105.

    PubMed Central  PubMed  Google Scholar 

  104. Mari F, Zelmann R, Andrade-Valenca L, et al. Continuous high-frequency activity in mesial temporal lobe structures. Epilepsia 2012;53:797-806.

    PubMed Central  PubMed  Google Scholar 

  105. Melani F, Zelmann R, Mari F, Gotman J. Continuous high frequency activity: a peculiar SEEG pattern related to specific brain regions. Clin Neurophysiol 2013;124:1507-1516.

    PubMed  Google Scholar 

  106. Kobayashi K, Jacobs J, Gotman J. Detection of changes of high-frequency activity by statistical time-frequency analysis in epileptic spikes. Clin Neurophysiol 2009;120:1070-1077.

    PubMed Central  PubMed  Google Scholar 

  107. Wieser HG, Bancaud J, Talairach J, et al. Comparative value of spontaneous and chemically and electrically induced seizures in establishing the lateralization of temporal lobe seizures. Epilepsia 1979;20:47-59.

    CAS  PubMed  Google Scholar 

  108. Lieb JP, Joseph JP, Engel J, Jr., et al. Sleep state and seizure foci related to depth spike activity in patients with temporal lobe epilepsy. Electroencephalogr Clin Neurophysiol 1980;49:538-557.

    CAS  PubMed  Google Scholar 

  109. Sammaritano M, Gigli GL, Gotman J. Interictal spiking during wakefulness and sleep and the localization of foci in temporal lobe epilepsy. Neurology 1991;41:290-297.

    CAS  PubMed  Google Scholar 

  110. Wang S, Wang IZ, Bulacio JC, et al. Ripple classification helps to localize the seizure-onset zone in neocortical epilepsy. Epilepsia 2013;54:370-376.

    PubMed  Google Scholar 

  111. Jacobs J, Zijlmans M, Zelmann R, et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol 2010;67:209-220.

    PubMed Central  PubMed  Google Scholar 

  112. Zijlmans M, Jacobs J, Kahn YU, et al. Ictal and interictal high frequency oscillations in patients with focal epilepsy. Clin Neurophysiol 2011;122:664-671.

    PubMed Central  PubMed  Google Scholar 

  113. Jacobs J, Zijlmans M, Zelmann R, et al. Value of electrical stimulation and high frequency oscillations (80–500 Hz) in identifying epileptogenic areas during intracranial EEG recordings. Epilepsia 2010;51:573-582.

    PubMed Central  PubMed  Google Scholar 

  114. Bragin A, Wilson CL, Engel JJ. Spatial stability over time of brain areas generating fast ripples in the epileptic rat. Epilepsia 2003;44:1233-1237.

    PubMed  Google Scholar 

  115. Kobayashi K, Watanabe Y, Inoue T, et al. Scalp-recorded high-frequency oscillations in childhood sleep-induced electrical status epilepticus. Epilepsia 2010;51:2190-2194.

    PubMed  Google Scholar 

  116. Andrade-Valenca LP, Dubeau F, Mari F, et al. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology 2011;77:524-531.

    CAS  PubMed Central  PubMed  Google Scholar 

  117. Melani F, Zelmann R, Dubeau F, Gotman J. Occurrence of scalp-fast oscillations among patients with different spiking rate and their role as epileptogenicity marker. Epilepsy Res 2013;106:345-356.

    PubMed  Google Scholar 

  118. Park SC, Lee SK, Che H, et al. Ictal high-gamma oscillation (60-99 Hz) in intracranial electroencephalography and postoperative seizure outcome in neocortical epilepsy. Clin Neurophysiol. 2012;123:1100-1110.

    Google Scholar 

  119. Wu JY, Sankar R, Lerner JT, et al. Removing interictal fast ripples on electrocorticography linked with seizure freedom in children. Neurology 2010;75:1686-1694.

    CAS  PubMed Central  PubMed  Google Scholar 

  120. Cho JR, Joo EY, Koo DL, et al. Clinical utility of interictal high-frequency oscillations recorded with subdural macroelectrodes in partial epilepsy. J Clin Neurol 2012;8:22-34.

    PubMed Central  PubMed  Google Scholar 

  121. Haegelen C, Perucca P, Chatillon CE, et al. High-frequency oscillations, extent of surgical resection, and surgical outcome in drug-resistant focal epilepsy. Epilepsia 2013;54:848-857.

    PubMed Central  PubMed  Google Scholar 

  122. van ’t Klooster MA, Zijlmans M, Leijten FS, et al. Time-frequency analysis of single pulse electrical stimulation to assist delineation of epileptogenic cortex. Brain 2011;134:2855-2866.

    Google Scholar 

  123. Wetjen NM, Marsh WR, Meyer FB, et al. Intracranial electroencephalography seizure onset patterns and surgical outcomes in nonlesional extratemporal epilepsy. J Neurosurg 2009;110:1147-1152.

    PubMed Central  PubMed  Google Scholar 

  124. Fujiwara H, Greiner HM, Lee KH, et al. Resection of ictal high-frequency oscillations leads to favorable surgical outcome in pediatric epilepsy. Epilepsia 2012;53:1607-1617.

    PubMed Central  PubMed  Google Scholar 

  125. Usui N, Terada K, Baba K, et al. Clinical significance of ictal high frequency oscillations in medial temporal lobe epilepsy. Clin Neurophysiol 2011;122:1693-1700.

    PubMed  Google Scholar 

  126. Modur PN, Zhang S, Vitaz TW. Ictal high-frequency oscillations in neocortical epilepsy: implications for seizure localization and surgical resection. Epilepsia 2011;52:1792-1801.

    PubMed Central  PubMed  Google Scholar 

  127. Williams PA, White AM, Clark S, et al. Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J Neurosci 2009;29:2103-2112.

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Levesque M, Bortel A, Gotman J, Avoli M. High-frequency (80–500 Hz) oscillations and epileptogenesis in temporal lobe epilepsy. Neurobiol Dis 2011;42:231-241.

    PubMed  Google Scholar 

Download references

Acknowledgments

RJS is funded by NINDS NS R01-071048, MS NINDS NS R01-78136, and GAW NINDS NS R01-63039.

Required Author Forms

Disclosure forms provided by the authors are available with the online version of this article.

Author information

Authors and Affiliations

  1. David Geffen School of Medicine at UCLA, Department of Neurology, Room 2-155, 710 Westwood Plaza, Los Angeles, CA, 90095, USA

    Richard J. Staba

  2. Mayo Systems Electrophysiology Laboratory, Divisions of Child & Adolescent Neurology and Movement Disorders, Department of Neurology, Mayo Clinic, Rochester, MN, 55905, USA

    Matt Stead

  3. Mayo Systems Electrophysiology Laboratory, Divisions of Epilepsy and Clinical Neurophysiology, Departments of Neurology, Physiology and Bioengineering, Mayo Clinic, Rochester, MN, 55905, USA

    Gregory A. Worrell

Authors
  1. Richard J. Staba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matt Stead
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregory A. Worrell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard J. Staba.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 1.19 mb)

ESM 2

(PDF 1.19 mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Staba, R.J., Stead, M. & Worrell, G.A. Electrophysiological Biomarkers of Epilepsy. Neurotherapeutics 11, 334–346 (2014). https://doi.org/10.1007/s13311-014-0259-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13311-014-0259-0

Keywords

Search

Navigation