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24-11-2023 | Epilepsy | Review

Pathological and Physiological High-frequency Oscillations on Electroencephalography in Patients with Epilepsy

Authors: Hongyi Ye, Cong Chen, Shennan A. Weiss, Shuang Wang

Published in: Neuroscience Bulletin

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Abstract

High-frequency oscillations (HFOs) encompass ripples (80 Hz–200 Hz) and fast ripples (200 Hz–600 Hz), serving as a promising biomarker for localizing the epileptogenic zone in epilepsy. Spontaneous fast ripples are always pathological, while ripples may be physiological or pathological. Distinguishing physiological from pathological ripples is important not only for designating epileptogenic brain regions, but also for investigations that study ripples in the context of memory encoding, consolidation, and recall in patients with epilepsy. Many studies have sought to identify distinguishing features between pathological and physiological ripples over the past two decades. Physiological and pathological ripples differ with respect to their spatial location, cellular mechanisms, morphology, and coupling with background electroencephalographic activity. Retrospective studies have demonstrated that differentiating between pathological and physiological ripples can improve surgical outcome prediction. In this review, we summarize the characteristics, differences, and applications of pathological and physiological HFOs and discuss strategies for their clinical translation.
Literature
1.
go back to reference Fiest KM, Sauro KM, Wiebe S, Patten SB, Kwon CS, Dykeman J. Prevalence and incidence of epilepsy: A systematic review and meta-analysis of international studies. Neurology 2017, 88: 296–303.PubMedPubMedCentralCrossRef Fiest KM, Sauro KM, Wiebe S, Patten SB, Kwon CS, Dykeman J. Prevalence and incidence of epilepsy: A systematic review and meta-analysis of international studies. Neurology 2017, 88: 296–303.PubMedPubMedCentralCrossRef
2.
go back to reference Sultana B, Panzini MA, Veilleux Carpentier A, Comtois J, Rioux B, Gore G, et al. Incidence and prevalence of drug-resistant epilepsy: A systematic review and meta-analysis. Neurology 2021, 96: 805–817.PubMedCrossRef Sultana B, Panzini MA, Veilleux Carpentier A, Comtois J, Rioux B, Gore G, et al. Incidence and prevalence of drug-resistant epilepsy: A systematic review and meta-analysis. Neurology 2021, 96: 805–817.PubMedCrossRef
3.
go back to reference Lüders HO, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: General principles. Epileptic Disord 2006, 8: S1–S9.PubMedCrossRef Lüders HO, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: General principles. Epileptic Disord 2006, 8: S1–S9.PubMedCrossRef
4.
go back to reference Frauscher B, Bartolomei F, Kobayashi K, Cimbalnik J, van’t Klooster MA, Rampp S, et al. High-frequency oscillations: The state of clinical research. Epilepsia 2017, 58: 1316–1329.PubMedPubMedCentralCrossRef Frauscher B, Bartolomei F, Kobayashi K, Cimbalnik J, van’t Klooster MA, Rampp S, et al. High-frequency oscillations: The state of clinical research. Epilepsia 2017, 58: 1316–1329.PubMedPubMedCentralCrossRef
5.
go back to reference Chen Z, Maturana MI, Burkitt AN, Cook MJ, Grayden DB. High-frequency oscillations in epilepsy: What have we learned and what needs to be addressed. Neurology 2021, 96: 439–448.PubMedCrossRef Chen Z, Maturana MI, Burkitt AN, Cook MJ, Grayden DB. High-frequency oscillations in epilepsy: What have we learned and what needs to be addressed. Neurology 2021, 96: 439–448.PubMedCrossRef
6.
go back to reference Jacobs J, LeVan P, Chander R, Hall J, Dubeau F, Gotman J. Interictal high-frequency oscillations (80 Hz–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia 2008, 49: 1893–1907.PubMedPubMedCentralCrossRef Jacobs J, LeVan P, Chander R, Hall J, Dubeau F, Gotman J. Interictal high-frequency oscillations (80 Hz–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia 2008, 49: 1893–1907.PubMedPubMedCentralCrossRef
7.
go back to reference Jacobs J, Zijlmans M, Zelmann R, Chatillon CE, Hall J, Olivier A, et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol 2010, 67: 209–220.PubMedPubMedCentralCrossRef Jacobs J, Zijlmans M, Zelmann R, Chatillon CE, Hall J, Olivier A, et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol 2010, 67: 209–220.PubMedPubMedCentralCrossRef
8.
go back to reference Zweiphenning W, van’t Klooster MA, van Klink NEC, Leijten FSS, Ferrier CH, Gebbink T, et al. Intraoperative electrocorticography using high-frequency oscillations or spikes to tailor epilepsy surgery in the Netherlands (the HFO trial): A randomised, single-blind, adaptive non-inferiority trial. Lancet Neurol 2022, 21: 982–993.PubMedPubMedCentralCrossRef Zweiphenning W, van’t Klooster MA, van Klink NEC, Leijten FSS, Ferrier CH, Gebbink T, et al. Intraoperative electrocorticography using high-frequency oscillations or spikes to tailor epilepsy surgery in the Netherlands (the HFO trial): A randomised, single-blind, adaptive non-inferiority trial. Lancet Neurol 2022, 21: 982–993.PubMedPubMedCentralCrossRef
9.
go back to reference Staba RJ, Wilson CL, Bragin A, Jhung D, Fried I, Engel J Jr. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann Neurol 2004, 56: 108–115.PubMedCrossRef Staba RJ, Wilson CL, Bragin A, Jhung D, Fried I, Engel J Jr. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann Neurol 2004, 56: 108–115.PubMedCrossRef
10.
go back to reference Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus 1999, 9: 137–142.PubMedCrossRef Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus 1999, 9: 137–142.PubMedCrossRef
12.
go back to reference Bragin A, Engel J, 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 1999, 40: 127–137.PubMedCrossRef Bragin A, Engel J, 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 1999, 40: 127–137.PubMedCrossRef
13.
go back to reference Jiruska P, Alvarado-Rojas C, Schevon CA, Staba R, Stacey W, Wendling F, et al. Update on the mechanisms and roles of high-frequency oscillations in seizures and epileptic disorders. Epilepsia 2017, 58: 1330–1339.PubMedPubMedCentralCrossRef Jiruska P, Alvarado-Rojas C, Schevon CA, Staba R, Stacey W, Wendling F, et al. Update on the mechanisms and roles of high-frequency oscillations in seizures and epileptic disorders. Epilepsia 2017, 58: 1330–1339.PubMedPubMedCentralCrossRef
14.
go back to reference Frauscher B, von Ellenrieder N, Zelmann R, Rogers C, Nguyen DK, Kahane P, et al. High-frequency oscillations in the normal human brain. Ann Neurol 2018, 84: 374–385.PubMedCrossRef Frauscher B, von Ellenrieder N, Zelmann R, Rogers C, Nguyen DK, Kahane P, et al. High-frequency oscillations in the normal human brain. Ann Neurol 2018, 84: 374–385.PubMedCrossRef
15.
go back to reference Li L, Kumar U, You J, Zhou Y, Weiss SA, Engel J, et al. Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis. Neurobiol Dis 2021, 161: 105544.PubMedPubMedCentralCrossRef Li L, Kumar U, You J, Zhou Y, Weiss SA, Engel J, et al. Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis. Neurobiol Dis 2021, 161: 105544.PubMedPubMedCentralCrossRef
16.
go back to reference Bragin A, Li L, Almajano J, Alvarado-Rojas C, Reid AY, Staba RJ, et al. Pathologic electrographic changes after experimental traumatic brain injury. Epilepsia 2016, 57: 735–745.PubMedPubMedCentralCrossRef Bragin A, Li L, Almajano J, Alvarado-Rojas C, Reid AY, Staba RJ, et al. Pathologic electrographic changes after experimental traumatic brain injury. Epilepsia 2016, 57: 735–745.PubMedPubMedCentralCrossRef
18.
go back to reference Frauscher B, von Ellenrieder N, Zelmann R, Doležalová I, Minotti L, Olivier A, et al. Atlas of the normal intracranial electroencephalogram: Neurophysiological awake activity in different cortical areas. Brain 2018, 141: 1130–1144.PubMedCrossRef Frauscher B, von Ellenrieder N, Zelmann R, Doležalová I, Minotti L, Olivier A, et al. Atlas of the normal intracranial electroencephalogram: Neurophysiological awake activity in different cortical areas. Brain 2018, 141: 1130–1144.PubMedCrossRef
19.
go back to reference Zweiphenning WJEM, von Ellenrieder N, Dubeau F, Martineau L, Minotti L, Hall JA, et al. Correcting for physiological ripples improves epileptic focus identification and outcome prediction. Epilepsia 2022, 63: 483–496.PubMedCrossRef Zweiphenning WJEM, von Ellenrieder N, Dubeau F, Martineau L, Minotti L, Hall JA, et al. Correcting for physiological ripples improves epileptic focus identification and outcome prediction. Epilepsia 2022, 63: 483–496.PubMedCrossRef
20.
go back to reference Engel J, Bragin A, Staba R, Mody I. High-frequency oscillations: What is normal and what is not? Epilepsia 2009, 50: 598–604.PubMedCrossRef Engel J, Bragin A, Staba R, Mody I. High-frequency oscillations: What is normal and what is not? Epilepsia 2009, 50: 598–604.PubMedCrossRef
21.
go back to reference Frauscher B, Gotman J. How can I disentangle physiological and pathological high-frequency oscillations. In: Studies in Neuroscience Psychology and Behavioral Economics, Springer, Cham, 2023, pp 377–388. Frauscher B, Gotman J. How can I disentangle physiological and pathological high-frequency oscillations. In: Studies in Neuroscience Psychology and Behavioral Economics, Springer, Cham, 2023, pp 377–388.
22.
go back to reference Liu AA, Henin S, Abbaspoor S, Bragin A, Buffalo EA, Farrell JS, et al. A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations. Nat Commun 2022, 13: 6000.PubMedPubMedCentralCrossRef Liu AA, Henin S, Abbaspoor S, Bragin A, Buffalo EA, Farrell JS, et al. A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations. Nat Commun 2022, 13: 6000.PubMedPubMedCentralCrossRef
23.
go back to reference Zijlmans M, Worrell GA, Dümpelmann M, Stieglitz T, Barborica A, Heers M, et al. How to record high-frequency oscillations in epilepsy: A practical guideline. Epilepsia 2017, 58: 1305–1315.PubMedCrossRef Zijlmans M, Worrell GA, Dümpelmann M, Stieglitz T, Barborica A, Heers M, et al. How to record high-frequency oscillations in epilepsy: A practical guideline. Epilepsia 2017, 58: 1305–1315.PubMedCrossRef
24.
go back to reference Noorlag L, van Klink NEC, Kobayashi K, Gotman J, Braun KPJ, Zijlmans M. High-frequency oscillations in scalp EEG: A systematic review of methodological choices and clinical findings. Clin Neurophysiol 2022, 137: 46–58.PubMedCrossRef Noorlag L, van Klink NEC, Kobayashi K, Gotman J, Braun KPJ, Zijlmans M. High-frequency oscillations in scalp EEG: A systematic review of methodological choices and clinical findings. Clin Neurophysiol 2022, 137: 46–58.PubMedCrossRef
25.
go back to reference Gardner AB, Worrell GA, Marsh E, Dlugos D, Litt B. Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings. Clin Neurophysiol 2007, 118: 1134–1143.PubMedPubMedCentralCrossRef Gardner AB, Worrell GA, Marsh E, Dlugos D, Litt B. Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings. Clin Neurophysiol 2007, 118: 1134–1143.PubMedPubMedCentralCrossRef
26.
go back to reference Spring AM, Pittman DJ, Aghakhani Y, Jirsch J, Pillay N, Bello-Espinosa LE, et al. Interrater reliability of visually evaluated high frequency oscillations. Clin Neurophysiol 2017, 128: 433–441.PubMedCrossRef Spring AM, Pittman DJ, Aghakhani Y, Jirsch J, Pillay N, Bello-Espinosa LE, et al. Interrater reliability of visually evaluated high frequency oscillations. Clin Neurophysiol 2017, 128: 433–441.PubMedCrossRef
27.
go back to reference Nariai H, Wu JY, Bernardo D, Fallah A, Sankar R, Hussain SA. Interrater reliability in visual identification of interictal high-frequency oscillations on electrocorticography and scalp EEG. Epilepsia Open 2018, 3: 127–132.PubMedPubMedCentralCrossRef Nariai H, Wu JY, Bernardo D, Fallah A, Sankar R, Hussain SA. Interrater reliability in visual identification of interictal high-frequency oscillations on electrocorticography and scalp EEG. Epilepsia Open 2018, 3: 127–132.PubMedPubMedCentralCrossRef
28.
go back to reference Bénar CG, Chauvière 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.PubMedCrossRef Bénar CG, Chauvière 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.PubMedCrossRef
29.
go back to reference Chaibi S, Lajnef T, Sakka Z, Samet M, Kachouri A. A reliable approach to distinguish between transient with and without HFOs using TQWT and MCA. J Neurosci Methods 2014, 232: 36–46.PubMedCrossRef Chaibi S, Lajnef T, Sakka Z, Samet M, Kachouri A. A reliable approach to distinguish between transient with and without HFOs using TQWT and MCA. J Neurosci Methods 2014, 232: 36–46.PubMedCrossRef
30.
go back to reference Weiss SA, Berry B, Chervoneva I, Waldman Z, Guba J, Bower M, et al. Visually validated semi-automatic high-frequency oscillation detection aides the delineation of epileptogenic regions during intra-operative electrocorticography. Clin Neurophysiol 2018, 129: 2089–2098.PubMedCrossRef Weiss SA, Berry B, Chervoneva I, Waldman Z, Guba J, Bower M, et al. Visually validated semi-automatic high-frequency oscillation detection aides the delineation of epileptogenic regions during intra-operative electrocorticography. Clin Neurophysiol 2018, 129: 2089–2098.PubMedCrossRef
32.
go back to reference Henin S, Shankar A, Borges H, Flinker A, Doyle W, Friedman D, et al. Spatiotemporal dynamics between interictal epileptiform discharges and ripples during associative memory processing. Brain 2021, 144: 1590–1602.PubMedPubMedCentralCrossRef Henin S, Shankar A, Borges H, Flinker A, Doyle W, Friedman D, et al. Spatiotemporal dynamics between interictal epileptiform discharges and ripples during associative memory processing. Brain 2021, 144: 1590–1602.PubMedPubMedCentralCrossRef
33.
go back to reference Norman Y, Yeagle EM, Khuvis S, Harel M, Mehta AD, Malach R. Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. Science 2019, 365: eaax1030.PubMedCrossRef Norman Y, Yeagle EM, Khuvis S, Harel M, Mehta AD, Malach R. Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. Science 2019, 365: eaax1030.PubMedCrossRef
34.
go back to reference Vaz AP, Inati SK, Brunel N, Zaghloul KA. Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory. Science 2019, 363: 975–978.PubMedPubMedCentralCrossRef Vaz AP, Inati SK, Brunel N, Zaghloul KA. Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory. Science 2019, 363: 975–978.PubMedPubMedCentralCrossRef
35.
go back to reference Matsumoto A, Brinkmann BH, Matthew Stead S, Matsumoto J, Kucewicz MT, Marsh WR, et al. Pathological and physiological high-frequency oscillations in focal human epilepsy. J Neurophysiol 2013, 110: 1958–1964.PubMedPubMedCentralCrossRef Matsumoto A, Brinkmann BH, Matthew Stead S, Matsumoto J, Kucewicz MT, Marsh WR, et al. Pathological and physiological high-frequency oscillations in focal human epilepsy. J Neurophysiol 2013, 110: 1958–1964.PubMedPubMedCentralCrossRef
36.
go back to reference Frauscher B, von Ellenrieder N, Ferrari-Marinho T, Avoli M, Dubeau F, Gotman J. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain 2015, 138: 1629–1641.PubMedPubMedCentralCrossRef Frauscher B, von Ellenrieder N, Ferrari-Marinho T, Avoli M, Dubeau F, Gotman J. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain 2015, 138: 1629–1641.PubMedPubMedCentralCrossRef
37.
go back to reference von Ellenrieder N, Frauscher B, Dubeau F, Gotman J. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high-frequency oscillations (80–500 Hz). Epilepsia 2016, 57: 869–878.CrossRef von Ellenrieder N, Frauscher B, Dubeau F, Gotman J. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high-frequency oscillations (80–500 Hz). Epilepsia 2016, 57: 869–878.CrossRef
38.
go back to reference Song I, Orosz I, Chervoneva I, Waldman ZJ, Fried I, Wu C, et al. Bimodal coupling of ripples and slower oscillations during sleep in patients with focal epilepsy. Epilepsia 2017, 58: 1972–1984.PubMedPubMedCentralCrossRef Song I, Orosz I, Chervoneva I, Waldman ZJ, Fried I, Wu C, et al. Bimodal coupling of ripples and slower oscillations during sleep in patients with focal epilepsy. Epilepsia 2017, 58: 1972–1984.PubMedPubMedCentralCrossRef
39.
go back to reference Chen C, Wang Y, Ye L, Xu J, Ming W, Liu X, et al. A region-specific modulation of sleep slow waves on interictal epilepsy markers in focal epilepsy. Epilepsia 2023, 64: 973–985.PubMedCrossRef Chen C, Wang Y, Ye L, Xu J, Ming W, Liu X, et al. A region-specific modulation of sleep slow waves on interictal epilepsy markers in focal epilepsy. Epilepsia 2023, 64: 973–985.PubMedCrossRef
40.
go back to reference Kerber K, Dümpelmann M, Schelter B, Le Van P, Korinthenberg R, Schulze-Bonhage A, et al. Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures. Clin Neurophysiol 2014, 125: 1339–1345.PubMedCrossRef Kerber K, Dümpelmann M, Schelter B, Le Van P, Korinthenberg R, Schulze-Bonhage A, et al. Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures. Clin Neurophysiol 2014, 125: 1339–1345.PubMedCrossRef
41.
go back to reference de Curtis M, Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 2001, 63: 541–567.PubMedCrossRef de Curtis M, Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 2001, 63: 541–567.PubMedCrossRef
42.
go back to reference Pail M, Cimbálník J, Roman R, Daniel P, Shaw DJ, Chrastina J, et al. High frequency oscillations in epileptic and non-epileptic human hippocampus during a cognitive task. Sci Rep 2020, 10: 18147.PubMedPubMedCentralCrossRef Pail M, Cimbálník J, Roman R, Daniel P, Shaw DJ, Chrastina J, et al. High frequency oscillations in epileptic and non-epileptic human hippocampus during a cognitive task. Sci Rep 2020, 10: 18147.PubMedPubMedCentralCrossRef
43.
go back to reference Wang S, Wang IZ, Bulacio JC, Mosher JC, Gonzalez-Martinez J, Alexopoulos AV, et al. Ripple classification helps to localize the seizure-onset zone in neocortical epilepsy. Epilepsia 2013, 54: 370–376.PubMedCrossRef Wang S, Wang IZ, Bulacio JC, Mosher JC, Gonzalez-Martinez J, Alexopoulos AV, et al. Ripple classification helps to localize the seizure-onset zone in neocortical epilepsy. Epilepsia 2013, 54: 370–376.PubMedCrossRef
44.
go back to reference von Ellenrieder N, Dubeau F, Gotman J, Frauscher B. Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. Neuroimage Clin 2017, 14: 566–573.CrossRef von Ellenrieder N, Dubeau F, Gotman J, Frauscher B. Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. Neuroimage Clin 2017, 14: 566–573.CrossRef
45.
go back to reference Ferrari-Marinho T, Perucca P, Mok K, Olivier A, Hall J, Dubeau F, et al. Pathologic substrates of focal epilepsy influence the generation of high-frequency oscillations. Epilepsia 2015, 56: 592–598.PubMedCrossRef Ferrari-Marinho T, Perucca P, Mok K, Olivier A, Hall J, Dubeau F, et al. Pathologic substrates of focal epilepsy influence the generation of high-frequency oscillations. Epilepsia 2015, 56: 592–598.PubMedCrossRef
46.
go back to reference Jefferys JGR, Menendez de la Prida L, Wendling F, Bragin A, Avoli M, Timofeev I, et al. Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol 2012, 98: 250–264.PubMedPubMedCentralCrossRef Jefferys JGR, Menendez de la Prida L, Wendling F, Bragin A, Avoli M, Timofeev I, et al. Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol 2012, 98: 250–264.PubMedPubMedCentralCrossRef
47.
go back to reference Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J Neurosci 1995, 15: 30–46.PubMedPubMedCentralCrossRef Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J Neurosci 1995, 15: 30–46.PubMedPubMedCentralCrossRef
48.
go back to reference Schomburg EW, Anastassiou CA, Buzsáki G, Koch C. The spiking component of oscillatory extracellular potentials in the rat hippocampus. J Neurosci 2012, 32: 11798–11811.PubMedPubMedCentralCrossRef Schomburg EW, Anastassiou CA, Buzsáki G, Koch C. The spiking component of oscillatory extracellular potentials in the rat hippocampus. J Neurosci 2012, 32: 11798–11811.PubMedPubMedCentralCrossRef
49.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
50.
go back to reference Weiss SA, Sheybani L, Seenarine N, Fried I, Wu C, Sharan A, et al. Delta oscillation coupled propagating fast ripples precede epileptiform discharges in patients with focal epilepsy. Neurobiol Dis 2022, 175: 105928.PubMedCrossRef Weiss SA, Sheybani L, Seenarine N, Fried I, Wu C, Sharan A, et al. Delta oscillation coupled propagating fast ripples precede epileptiform discharges in patients with focal epilepsy. Neurobiol Dis 2022, 175: 105928.PubMedCrossRef
51.
go back to reference Cimbalnik J, Brinkmann B, Kremen V, Jurak P, Berry B, Gompel JV, et al. Physiological and pathological high frequency oscillations in focal epilepsy. Ann Clin Transl Neurol 2018, 5: 1062–1076.PubMedPubMedCentralCrossRef Cimbalnik J, Brinkmann B, Kremen V, Jurak P, Berry B, Gompel JV, et al. Physiological and pathological high frequency oscillations in focal epilepsy. Ann Clin Transl Neurol 2018, 5: 1062–1076.PubMedPubMedCentralCrossRef
52.
go back to reference Karpychev V, Balatskaya A, Utyashev N, Pedyash N, Zuev A, Dragoy O, et al. Epileptogenic high-frequency oscillations present larger amplitude both in mesial temporal and neocortical regions. Front Hum Neurosci 2022, 16: 984306.PubMedPubMedCentralCrossRef Karpychev V, Balatskaya A, Utyashev N, Pedyash N, Zuev A, Dragoy O, et al. Epileptogenic high-frequency oscillations present larger amplitude both in mesial temporal and neocortical regions. Front Hum Neurosci 2022, 16: 984306.PubMedPubMedCentralCrossRef
53.
go back to reference Malinowska U, Badier JM, Gavaret M, Bartolomei F, Chauvel P, Bénar CG. Interictal networks in magnetoencephalography. Hum Brain Mapp 2014, 35: 2789–2805.PubMedCrossRef Malinowska U, Badier JM, Gavaret M, Bartolomei F, Chauvel P, Bénar CG. Interictal networks in magnetoencephalography. Hum Brain Mapp 2014, 35: 2789–2805.PubMedCrossRef
54.
go back to reference Alkawadri R, Gaspard N, Goncharova II, Spencer DD, Gerrard JL, Zaveri H, et al. The spatial and signal characteristics of physiologic high frequency oscillations. Epilepsia 2014, 55: 1986–1995.PubMedPubMedCentralCrossRef Alkawadri R, Gaspard N, Goncharova II, Spencer DD, Gerrard JL, Zaveri H, et al. The spatial and signal characteristics of physiologic high frequency oscillations. Epilepsia 2014, 55: 1986–1995.PubMedPubMedCentralCrossRef
55.
go back to reference Liu S, Gurses C, Sha Z, Quach MM, Sencer A, Bebek N, et al. Stereotyped high-frequency oscillations discriminate seizure onset zones and critical functional cortex in focal epilepsy. Brain 2018, 141: 713–730.PubMedPubMedCentralCrossRef Liu S, Gurses C, Sha Z, Quach MM, Sencer A, Bebek N, et al. Stereotyped high-frequency oscillations discriminate seizure onset zones and critical functional cortex in focal epilepsy. Brain 2018, 141: 713–730.PubMedPubMedCentralCrossRef
56.
go back to reference Guragain H, Cimbalnik J, Stead M, Groppe DM, Berry BM, Kremen V, et al. Spatial variation in high-frequency oscillation rates and amplitudes in intracranial EEG. Neurology 2018, 90: e639–e646.PubMedPubMedCentralCrossRef Guragain H, Cimbalnik J, Stead M, Groppe DM, Berry BM, Kremen V, et al. Spatial variation in high-frequency oscillation rates and amplitudes in intracranial EEG. Neurology 2018, 90: e639–e646.PubMedPubMedCentralCrossRef
57.
go back to reference Alvarado-Rojas C, Huberfeld G, Baulac M, Clemenceau S, Charpier S, Miles R, et al. Different mechanisms of ripple-like oscillations in the human epileptic subiculum. Ann Neurol 2015, 77: 281–290.PubMedCrossRef Alvarado-Rojas C, Huberfeld G, Baulac M, Clemenceau S, Charpier S, Miles R, et al. Different mechanisms of ripple-like oscillations in the human epileptic subiculum. Ann Neurol 2015, 77: 281–290.PubMedCrossRef
58.
go back to reference Crépon B, Navarro V, Hasboun D, Clemenceau S, Martinerie J, Baulac M, et al. Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. Brain 2010, 133: 33–45.PubMedCrossRef Crépon B, Navarro V, Hasboun D, Clemenceau S, Martinerie J, Baulac M, et al. Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. Brain 2010, 133: 33–45.PubMedCrossRef
59.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
60.
go back to reference Karoly PJ, Freestone DR, Boston R, Grayden DB, Himes D, Leyde K, et al. Interictal spikes and epileptic seizures: Their relationship and underlying rhythmicity. Brain 2016, 139: 1066–1078.PubMedCrossRef Karoly PJ, Freestone DR, Boston R, Grayden DB, Himes D, Leyde K, et al. Interictal spikes and epileptic seizures: Their relationship and underlying rhythmicity. Brain 2016, 139: 1066–1078.PubMedCrossRef
62.
go back to reference Weiss SA, Orosz I, Salamon N, Moy S, Wei L, Van’t Klooster MA, et al. Ripples on spikes show increased phase-amplitude coupling in mesial temporal lobe epilepsy seizure-onset zones. Epilepsia 2016, 57: 1916–1930.PubMedPubMedCentralCrossRef Weiss SA, Orosz I, Salamon N, Moy S, Wei L, Van’t Klooster MA, et al. Ripples on spikes show increased phase-amplitude coupling in mesial temporal lobe epilepsy seizure-onset zones. Epilepsia 2016, 57: 1916–1930.PubMedPubMedCentralCrossRef
63.
go back to reference Jacobs J, Vogt C, LeVan P, Zelmann R, Gotman J, Kobayashi K. The identification of distinct high-frequency oscillations during spikes delineates the seizure onset zone better than high-frequency spectral power changes. Clin Neurophysiol 2016, 127: 129–142.PubMedCrossRef Jacobs J, Vogt C, LeVan P, Zelmann R, Gotman J, Kobayashi K. The identification of distinct high-frequency oscillations during spikes delineates the seizure onset zone better than high-frequency spectral power changes. Clin Neurophysiol 2016, 127: 129–142.PubMedCrossRef
64.
go back to reference Schönberger J, Knopf A, Klotz KA, Dümpelmann M, Schulze-Bonhage A, Jacobs J. Distinction of physiologic and epileptic ripples: An electrical stimulation study. Brain Sci 2021, 11: 538.PubMedPubMedCentralCrossRef Schönberger J, Knopf A, Klotz KA, Dümpelmann M, Schulze-Bonhage A, Jacobs J. Distinction of physiologic and epileptic ripples: An electrical stimulation study. Brain Sci 2021, 11: 538.PubMedPubMedCentralCrossRef
65.
go back to reference Mooij AH, Huiskamp GJM, Aarts E, Ferrier CH, Braun KPJ, Zijlmans M. Accurate differentiation between physiological and pathological ripples recorded with scalp-EEG. Clin Neurophysiol 2022, 143: 172–181.PubMedCrossRef Mooij AH, Huiskamp GJM, Aarts E, Ferrier CH, Braun KPJ, Zijlmans M. Accurate differentiation between physiological and pathological ripples recorded with scalp-EEG. Clin Neurophysiol 2022, 143: 172–181.PubMedCrossRef
66.
go back to reference Cai Z, Sohrabpour A, Jiang H, Ye S, Joseph B, Brinkmann BH, et al. Noninvasive high-frequency oscillations riding spikes delineates epileptogenic sources. Proc Natl Acad Sci U S A 2021, 118: e2011130118.PubMedPubMedCentralCrossRef Cai Z, Sohrabpour A, Jiang H, Ye S, Joseph B, Brinkmann BH, et al. Noninvasive high-frequency oscillations riding spikes delineates epileptogenic sources. Proc Natl Acad Sci U S A 2021, 118: e2011130118.PubMedPubMedCentralCrossRef
67.
go back to reference Kramer MA, Ostrowski LM, Song DY, Thorn EL, Stoyell SM, Parnes M, et al. Scalp recorded spike ripples predict seizure risk in childhood epilepsy better than spikes. Brain 2019, 142: 1296–1309.PubMedPubMedCentralCrossRef Kramer MA, Ostrowski LM, Song DY, Thorn EL, Stoyell SM, Parnes M, et al. Scalp recorded spike ripples predict seizure risk in childhood epilepsy better than spikes. Brain 2019, 142: 1296–1309.PubMedPubMedCentralCrossRef
68.
go back to reference Weiss SA, Fried I, Engel J, Sperling MR, Wong RKS, Nir Y, et al. Fast ripples reflect increased excitability that primes epileptiform spikes. Brain Commun 2023, 5: fcad242.PubMedPubMedCentralCrossRef Weiss SA, Fried I, Engel J, Sperling MR, Wong RKS, Nir Y, et al. Fast ripples reflect increased excitability that primes epileptiform spikes. Brain Commun 2023, 5: fcad242.PubMedPubMedCentralCrossRef
69.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
70.
71.
go back to reference Weiss SA, Song I, Leng M, Pastore T, Slezak D, Waldman Z, et al. Ripples have distinct spectral properties and phase-amplitude coupling with slow waves, but indistinct unit firing, in human epileptogenic hippocampus. Front Neurol 2020, 11: 174.PubMedPubMedCentralCrossRef Weiss SA, Song I, Leng M, Pastore T, Slezak D, Waldman Z, et al. Ripples have distinct spectral properties and phase-amplitude coupling with slow waves, but indistinct unit firing, in human epileptogenic hippocampus. Front Neurol 2020, 11: 174.PubMedPubMedCentralCrossRef
72.
go back to reference Kuroda N, Sonoda M, Miyakoshi M, Nariai H, Jeong JW, Motoi H, et al. Objective interictal electrophysiology biomarkers optimize prediction of epilepsy surgery outcome. Brain Commun 2021, 3: fcabf42.CrossRef Kuroda N, Sonoda M, Miyakoshi M, Nariai H, Jeong JW, Motoi H, et al. Objective interictal electrophysiology biomarkers optimize prediction of epilepsy surgery outcome. Brain Commun 2021, 3: fcabf42.CrossRef
73.
go back to reference Ujma PP, Halász P, Kelemen A, Fabó D, Erőss L. Epileptic interictal discharges are more frequent during NREM slow wave downstates. Neurosci Lett 2017, 658: 37–42.PubMedCrossRef Ujma PP, Halász P, Kelemen A, Fabó D, Erőss L. Epileptic interictal discharges are more frequent during NREM slow wave downstates. Neurosci Lett 2017, 658: 37–42.PubMedCrossRef
74.
go back to reference Hay YA, Deperrois N, Fuchsberger T, Quarrell TM, Koerling AL, Paulsen O. Thalamus mediates neocortical Down state transition via GABAB-receptor-targeting interneurons. Neuron 2021, 109: 2682–2690.PubMedCrossRef Hay YA, Deperrois N, Fuchsberger T, Quarrell TM, Koerling AL, Paulsen O. Thalamus mediates neocortical Down state transition via GABAB-receptor-targeting interneurons. Neuron 2021, 109: 2682–2690.PubMedCrossRef
76.
go back to reference Nagasawa T, Juhász C, Rothermel R, Hoechstetter K, Sood S, Asano E. Spontaneous and visually driven high-frequency oscillations in the occipital cortex: Intracranial recording in epileptic patients. Hum Brain Mapp 2012, 33: 569–583.PubMedCrossRef Nagasawa T, Juhász C, Rothermel R, Hoechstetter K, Sood S, Asano E. Spontaneous and visually driven high-frequency oscillations in the occipital cortex: Intracranial recording in epileptic patients. Hum Brain Mapp 2012, 33: 569–583.PubMedCrossRef
77.
go back to reference Nonoda Y, Miyakoshi M, Ojeda A, Makeig S, Juhász C, Sood S, et al. Interictal high-frequency oscillations generated by seizure onset and eloquent areas may be differentially coupled with different slow waves. Clin Neurophysiol 2016, 127: 2489–2499.PubMedPubMedCentralCrossRef Nonoda Y, Miyakoshi M, Ojeda A, Makeig S, Juhász C, Sood S, et al. Interictal high-frequency oscillations generated by seizure onset and eloquent areas may be differentially coupled with different slow waves. Clin Neurophysiol 2016, 127: 2489–2499.PubMedPubMedCentralCrossRef
78.
go back to reference Clemens Z, Mölle M, Erőss L, Barsi P, Halász P, Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130: 2868–2878.PubMedCrossRef Clemens Z, Mölle M, Erőss L, Barsi P, Halász P, Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130: 2868–2878.PubMedCrossRef
79.
go back to reference Staresina BP, Bergmann TO, Bonnefond M, van der Meij R, Jensen O, Deuker L, et al. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci 2015, 18: 1679–1686.PubMedPubMedCentralCrossRef Staresina BP, Bergmann TO, Bonnefond M, van der Meij R, Jensen O, Deuker L, et al. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci 2015, 18: 1679–1686.PubMedPubMedCentralCrossRef
80.
go back to reference Bruder JC, Dümpelmann M, Piza DL, Mader M, Schulze-Bonhage A, Jacobs-Le Van J. Physiological ripples associated with sleep spindles differ in waveform morphology from epileptic ripples. Int J Neural Syst 2017, 27: 1750011.PubMedCrossRef Bruder JC, Dümpelmann M, Piza DL, Mader M, Schulze-Bonhage A, Jacobs-Le Van J. Physiological ripples associated with sleep spindles differ in waveform morphology from epileptic ripples. Int J Neural Syst 2017, 27: 1750011.PubMedCrossRef
81.
go back to reference Bruder JC, Schmelzeisen C, Lachner-Piza D, Reinacher P, Schulze-Bonhage A, Jacobs J. Physiological ripples associated with sleep spindles can be identified in patients with refractory epilepsy beyond mesio-temporal structures. Front Neurol 2021, 12: 612293.PubMedPubMedCentralCrossRef Bruder JC, Schmelzeisen C, Lachner-Piza D, Reinacher P, Schulze-Bonhage A, Jacobs J. Physiological ripples associated with sleep spindles can be identified in patients with refractory epilepsy beyond mesio-temporal structures. Front Neurol 2021, 12: 612293.PubMedPubMedCentralCrossRef
82.
go back to reference 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 1997, 17: 6783–6797.PubMedPubMedCentralCrossRef 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 1997, 17: 6783–6797.PubMedPubMedCentralCrossRef
83.
go back to reference Mak-McCully RA, Rolland M, Sargsyan A, Gonzalez C, Magnin M, Chauvel P, et al. Coordination of cortical and thalamic activity during non-REM sleep in humans. Nat Commun 2017, 8: 15499.PubMedPubMedCentralCrossRef Mak-McCully RA, Rolland M, Sargsyan A, Gonzalez C, Magnin M, Chauvel P, et al. Coordination of cortical and thalamic activity during non-REM sleep in humans. Nat Commun 2017, 8: 15499.PubMedPubMedCentralCrossRef
84.
go back to reference Wang S, So NK, Jin B, Wang IZ, Bulacio JC, Enatsu R, et al. Interictal ripples nested in epileptiform discharge help to identify the epileptogenic zone in neocortical epilepsy. Clin Neurophysiol 2017, 128: 945–951.PubMedCrossRef Wang S, So NK, Jin B, Wang IZ, Bulacio JC, Enatsu R, et al. Interictal ripples nested in epileptiform discharge help to identify the epileptogenic zone in neocortical epilepsy. Clin Neurophysiol 2017, 128: 945–951.PubMedCrossRef
85.
86.
go back to reference Weiss SA, Waldman Z, Raimondo F, Slezak D, Donmez M, Worrell G, et al. Localizing epileptogenic regions using high-frequency oscillations and machine learning. Biomark Med 2019, 13: 409–418.PubMedPubMedCentralCrossRef Weiss SA, Waldman Z, Raimondo F, Slezak D, Donmez M, Worrell G, et al. Localizing epileptogenic regions using high-frequency oscillations and machine learning. Biomark Med 2019, 13: 409–418.PubMedPubMedCentralCrossRef
87.
go back to reference Nevalainen P, von Ellenrieder N, Klimeš P, Dubeau F, Frauscher B, Gotman J. Association of fast ripples on intracranial EEG and outcomes after epilepsy surgery. Neurology 2020, 95: e2235–e2245.PubMedPubMedCentralCrossRef Nevalainen P, von Ellenrieder N, Klimeš P, Dubeau F, Frauscher B, Gotman J. Association of fast ripples on intracranial EEG and outcomes after epilepsy surgery. Neurology 2020, 95: e2235–e2245.PubMedPubMedCentralCrossRef
88.
go back to reference Roehri N, Pizzo F, Lagarde S, Lambert I, Nica A, McGonigal A, et al. High-frequency oscillations are not better biomarkers of epileptogenic tissues than spikes. Ann Neurol 2018, 83: 84–97.PubMedCrossRef Roehri N, Pizzo F, Lagarde S, Lambert I, Nica A, McGonigal A, et al. High-frequency oscillations are not better biomarkers of epileptogenic tissues than spikes. Ann Neurol 2018, 83: 84–97.PubMedCrossRef
89.
go back to reference Motoi H, Jeong JW, Juhász C, Miyakoshi M, Nakai Y, Sugiura A, et al. Quantitative analysis of intracranial electrocorticography signals using the concept of statistical parametric mapping. Sci Rep 2019, 9: 17385.PubMedPubMedCentralCrossRef Motoi H, Jeong JW, Juhász C, Miyakoshi M, Nakai Y, Sugiura A, et al. Quantitative analysis of intracranial electrocorticography signals using the concept of statistical parametric mapping. Sci Rep 2019, 9: 17385.PubMedPubMedCentralCrossRef
90.
go back to reference Weiss SA, Pastore T, Orosz I, Rubinstein D, Gorniak R, Waldman Z, et al. Graph theoretical measures of fast ripples support the epileptic network hypothesis. Brain Commun 2022, 4: fcac101.PubMedPubMedCentralCrossRef Weiss SA, Pastore T, Orosz I, Rubinstein D, Gorniak R, Waldman Z, et al. Graph theoretical measures of fast ripples support the epileptic network hypothesis. Brain Commun 2022, 4: fcac101.PubMedPubMedCentralCrossRef
91.
go back to reference Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia 2016, 57: 879–888.PubMedPubMedCentralCrossRef Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia 2016, 57: 879–888.PubMedPubMedCentralCrossRef
Metadata
Title
Pathological and Physiological High-frequency Oscillations on Electroencephalography in Patients with Epilepsy
Authors
Hongyi Ye
Cong Chen
Shennan A. Weiss
Shuang Wang
Publication date
24-11-2023
Publisher
Springer Nature Singapore
Published in
Neuroscience Bulletin
Print ISSN: 1673-7067
Electronic ISSN: 1995-8218
DOI
https://doi.org/10.1007/s12264-023-01150-6