Interictal high-frequency oscillations in focal human epilepsy
Language English Country England, Great Britain Media print
Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't, Review
Grant support
UH2 NS095495
NINDS NIH HHS - United States
UH2-NS095495
NINDS NIH HHS - United States
R01-NS092882
NINDS NIH HHS - United States
R01 NS063039
NINDS NIH HHS - United States
R01-NS063039
NINDS NIH HHS - United States
R01 NS092882
NINDS NIH HHS - United States
PubMed
26953850
PubMed Central
PMC4941960
DOI
10.1097/wco.0000000000000302
PII: 00019052-201604000-00011
Knihovny.cz E-resources
- MeSH
- Biomarkers analysis MeSH
- Electric Stimulation * methods MeSH
- Electroencephalography methods MeSH
- Epilepsies, Partial diagnosis physiopathology MeSH
- Humans MeSH
- Brain Mapping * MeSH
- Brain physiopathology MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Biomarkers MeSH
PURPOSE OF REVIEW: Localization of focal epileptic brain is critical for successful epilepsy surgery and focal brain stimulation. Despite significant progress, roughly half of all patients undergoing focal surgical resection, and most patients receiving focal electrical stimulation, are not seizure free. There is intense interest in high-frequency oscillations (HFOs) recorded with intracranial electroencephalography as potential biomarkers to improve epileptogenic brain localization, resective surgery, and focal electrical stimulation. The present review examines the evidence that HFOs are clinically useful biomarkers. RECENT FINDINGS: Performing the PubMed search 'High-Frequency Oscillations and Epilepsy' for 2013-2015 identifies 308 articles exploring HFO characteristics, physiological significance, and potential clinical applications. SUMMARY: There is strong evidence that HFOs are spatially associated with epileptic brain. There remain, however, significant challenges for clinical translation of HFOs as epileptogenic brain biomarkers: Differentiating true HFO from the high-frequency power changes associated with increased neuronal firing and bandpass filtering sharp transients. Distinguishing pathological HFO from normal physiological HFO. Classifying tissue under individual electrodes as normal or pathological. Sharing data and algorithms so research results can be reproduced across laboratories. Multicenter prospective trials to provide definitive evidence of clinical utility.
See more in PubMed
Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med. 2011;5:557–566. PubMed PMC
Jacobs J, Staba R, Asano E, et al. High frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol. 2012;98:302–315. PubMed PMC
Staba RJ, Stead M, Worrell GA. Electrophysiological biomarkers of epilepsy. Neurotherapeutics. 2014;11:334–346. This is a concise, up to date review of electrophysiological biomarkers in epilepsy. PubMed PMC
Urrestarazu E, Jirsch JD, LeVan P, et al. High-frequency intracerebral EEG activity (100–500 Hz) following interictal spikes. Epilepsia. 2006;47:1465–1476. PubMed
Najm I, Jehi L, Palmini A, et al. Temporal patterns and mechanisms of epilepsy surgery failure. Epilepsia. 2013;54:772–782. PubMed
Bergey GK, Morrell MJ, Mizrahi EM, et al. Long-term treatment with responsive brain stimulation in adults with refractory partial seizures. Neurology. 2015;84:810–817. This is a landmark paper describing the long-term follow-up of patients receiving focal brain stimulation using the NeuroPace responsive stimulation device. Previously, the class I evidence for efficacy was reported, and here the class IV evidence of a durable, improving, efficacy with focal stimulation. Over the course of 7 years, a significant number of patients had extended periods of seizure freedom, with 23% having at least 1 seizure-free period of more than 6 months and 12.9% with at least 1 seizure-free period more than 12 months, but no participants were seizure-free over the entire follow-up. PubMed PMC
Fisher RS, Webber WR, Lesser RP, et al. High-frequency EEG activity at the start of seizures. J Clin Neurophysiol. 1992;9:441–448. PubMed
Alarcon G, Binnie CD, Elwes RD, Polkey CE. Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. Electroencephalogr Clin Neurophysiol. 1995;94:326–337. PubMed
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
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. PubMed
Worrell GA, Parish L, Cranstoun SD, et al. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain. 2004;127(Pt 7):1496–1506. PubMed
Jirsch JD, Urrestarazu E, LeVan P, et al. High-frequency oscillations during human focal seizures. Brain. 2006;129(Pt 6):1593–1608. PubMed
Bragin A, Engel JJ, Wilson CL, et al. High-frequency oscillations in human brain. Hippocampus. 1999;9:137–142. PubMed
Bragin A, Engel JJ, Wilson CL, et al. Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia. 1999;40:1210–2121. PubMed
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
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
Worrell GA, Gardner AB, Stead SM, et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain. 2008;131(Pt 4):928–937. PubMed PMC
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 PMC
Jacobs J, Levan P, Châtillon CE, et al. High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. Brain. 2009;132(Pt 4):1022–1037. PubMed PMC
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 PMC
Zijlmans M, Jacobs J, Zelmann R, et al. High frequency oscillations and seizure frequency in patients with focal epilepsy. Epilepsy Res. 2009;85:287–292. PubMed PMC
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. PubMed PMC
van Klink NE, Van’t Klooster MA, Zelmann R, et al. High frequency oscillations in intra-operative electrocorticography before and after epilepsy surgery. Clin Neurophysiol. 2014;125:2212–2219. Observations that show fast ripples in intra-operative ECoG, compared to ripples, may be a better biomarker for epileptogenicity. Further studies are required to determine the relation between resection of epileptogenic tissue and physiological ripples generated by the sensorimotor cortex. PubMed
Cook MJ, O’Brien TJ, Berkovic SF, et al. Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: a first-in-man study. Lancet Neurol. 2013;12:563–571. PubMed
Brinkmann B. Crowdsourcing reproducible seizure forecasting in human and canine epilepsy. Brain. 2015 PubMed PMC
Pearce A, Wulsin D, Blanco JA, et al. Temporal changes of neocortical high frequency oscillations in epilepsy. J Neurophysiol. 2013;110:1167–1179. PubMed PMC
Alvarado-Rojas C, Valderrama M, Fouad-Ahmed A, et al. Slow modulations of high-frequency activity (40–140-Hz) discriminate preictal changes in human focal epilepsy. Sci Rep. 2014;4:4545–4543. PubMed PMC
Staba RJ, Bragin A. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: underlying mechanisms. Biomark Med. 2011;5:545–556. PubMed PMC
Worrell GA, Jerbi K, Kobayashi K, et al. Recording and analysis techniques for high-frequency oscillations. Prog Neurobiol. 2012;98:265–278. PubMed PMC
Ray S, Crone NE, Niebur E, et al. Neural correlates of high-gamma oscillations (60–200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J Neurosci. 2008;28:11526–11536. PubMed PMC
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. PubMed PMC
Waldert S, Lemon RN, Kraskov A. Influence of spiking activity on cortical local field potentials. J Physiol. 2013;591(Pt 21):5291–5303. PubMed PMC
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. PubMed
Engel J, Bragin A, Staba R, Mody I. High-frequency oscillations: what is normal and what is not? Epilepsia. 2009;50:598–604. PubMed
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 PMC
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
Buzsaki G, Horvath Z, Urioste R, et al. High-frequency network oscillaiton in hippocampus. Science. 1992;256:1025–1027. PubMed
Buzsáki G, Silva FL. High frequency oscillations in the intact brain. Prog Neurobiol. 2012;98:241–249. PubMed PMC
Buzsaki G. Rhythms of the brain. Oxford University Press; 2006.
Crone NE, Miglioretti DL, Gordon B, Lesser RP. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain. 1998;121(Pt 12):2301–2315. PubMed
Crone NE, Sinai A, Korzeniewska A. High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res. 2006;159:275–295. PubMed
Kucewicz MT, Worrell GA, Gotman J. Pathologic brain network activity: memory impairment in epilepsy. Neurology. 2013;81:12–13. PubMed PMC
Schevon CA, Trevelyan AJ, Schroeder CE, et al. Spatial characterization of interictal high frequency oscillations in epileptic neocortex. Brain. 2009;132(Pt 11):3047–3059. PubMed PMC
Blanco JA, Stead M, Krieger A, et al. Data mining neocortical high-frequency oscillations in epilepsy and controls. Brain. 2011;134(Pt 10):2948–2959. PubMed PMC
Haegelen C, Perucca P, Châtillon CE, et al. High-frequency oscillations, extent of surgical resection, and surgical outcome in drug-resistant focal epilepsy. Epilepsia. 2013;54:848–857. PubMed PMC
Burke JF, Ramayya AG, Kahana MJ. Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility? Curr Opin Neurobiol. 2014 A review of recent data supporting the view that HFA during memory processing is more consistent with an asynchronous signal, and can be used as a biomarker of neural activation to functionally map memory. PubMed PMC
Gibbs J. Letter to the Editor, Fourier’s series. Nature. 1899:59200.
Kucewicz MT, Cimbalnik J, Matsumoto JY, et al. High frequency oscillations are associated with cognitive processing in human recognition memory. Brain. 2014;137(Pt 8):2231–2244. This paper explores the spatial and temporal distribution of nHFO in a visual memory task. The study shows that high frequency oscillations are associated with memory processing and generated along distributed cortical and limbic brain regions. PubMed PMC
Jacobs J, Vogt C, LeVan P, et al. The identification of distinct high-frequency oscillations during spikes delineates the seizure onset zone better than high-frequency spectral power changes. Clin Neurophysiol. 2015;127:129–142. The rate of HFOs showed the best performance in identifying SOZ. PubMed
Gloor P. Contributions of electroencephalography and electrocorticography to the neurosurgical treatment of the epilepsies. Adv Neurol. 1975;8:59–105. PubMed
Le Van Quyen M, Khalilov I, Ben-Ari Y. The dark side of high-frequency oscillations in the developing brain. Trends Neurosci. 2006;29:419–427. PubMed
Alvarado-Rojas C, Huberfeld G, Baulac M, et al. Different mechanisms of ripple-like oscillations in the human epileptic subiculum. Ann Neurol. 2014;77:281–290. Many HFOs during interictal discharges and during pharmacologically induced preictal discharges preceding ictal-like events had frequencies more than 250 Hz, but also a significant proportion were spectrally similar to physiological ripples (150–250 Hz). Interestingly, preictal ripples were associated with depolarizing synaptic inputs frequently reaching the threshold for bursting in most pyramidal cells, suggesting that ripple oscillations (150–250 Hz) in human epileptic hippocampus are associated with two distinct population activities that rely on different cellular and synaptic mechanisms. Thus, the frequency of activity is not likely to be a reliable feature to distinguish pathological versus physiological HFO. PubMed PMC
Jefferys JG, Menendez de la Prida L, Wendling F, et al. Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol. 2012;98:250–264. PubMed PMC
Menendez de la Prida L, Staba RJ, Dian JA. Conundrums of high-frequency oscillations (80–800 Hz) in the epileptic brain. J Clin Neurophysiol. 2015;32:207–219. This invited review article is focused on the underlying complex neuronal events, that are not well understood, underlying pathological HFOs (80–800 Hz) PubMed PMC
Gulyás AI, Freund TT. Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation. Curr Opin Neurobiol. 2015;31:26–32. This article discusses evidence supporting that although physiological ripple oscillation is primarily the result of phasic perisomatic inhibitory currents, pathological high-frequency ripples are population spikes of partially synchronous, massively bursting, uninhibited pyramidal cells. PubMed
Chrobak JJ, Buzsaki G. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci. 1996;16:3056–3066. PubMed PMC
Logothetis NK, Kayser C, Oeltermann A. In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron. 2007;55:809–823. PubMed
Le Van Quyen M, Staba R, Bragin A, et al. Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. J Neurosci. 2010;30:7770–7782. PubMed PMC
Bragin A, Wilson CL, Almajano J, et al. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia. 2004;45:1017–1023. PubMed
Siegel AM, Cascino GD, Meyer FB, et al. Resective reoperation for failed epilepsy surgery: seizure outcome in 64 patients. Neurology. 2004;63:2298–2302. PubMed
Bell ML, Rao S, So EL, et al. Epilepsy surgery outcomes in temporal lobe epilepsy with a normal MRI. Epilepsia. 2009;50:2053–2060. PubMed PMC
Burkholder DB, Sulc V, Hoffman EM, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging-negative temporal lobe epilepsy surgery. JAMA Neurol. 2014;71:702–709. PubMed PMC
Noe K, Sulc V, Wong-Kisiel L, et al. Long-term outcomes after nonlesional extratemporal lobe epilepsy surgery. JAMA Neurol. 2013;70:1003–1008. PubMed PMC
Jones RT, Barth AM, Ormiston LD, Mody I. Evolution of temporal and spectral dynamics of pathologic high-frequency oscillations (pHFOs) during epileptogenesis. Epilepsia. 2015;56:1879–1889. This paper in a rat model of epileptogenesis demonstrates that hippocampal pHFOs exhibit a dynamic evolution during the epileptogenic period following status epilepticus, consistent with their role in transitioning to the chronic epilepsy. PubMed PMC
Engel J. Biomarkers in epilepsy: introduction. Biomark Med. 2011;5:537–544. PubMed
Gliske SV, Irwin ZT, Davis KA, et al. Universal automated high frequency oscillation detector for real-time, long term EEG. Clin Neurophysiol. 2015 (In press). This paper describes a detector for nterictal HFOs in intracranial EEG. The objective was to automatically remove false HFO detections related to artifacts, facilitating clinical use. These methods provide a strategy for real-time HFO detection in continuous EEG with minimal human monitoring of data quality. PubMed PMC
Button KS, Ioannidis JP, Mokrysz C, et al. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–376. PubMed
Ioannidis JP. Why most published research findings are false. PLoS medicine. 2005;2:e124. PubMed PMC
Landis SC, Amara SG, Asadullah K, et al. A call for transparent reporting to optimize the predictive value of preclinical research. Nature. 2012;490:187–191. PubMed PMC
Donoho DL. An invitation to reproducible computational research. Biostatistics. 2010;11:385–388. PubMed
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 PMC
van ’t Klooster MA, Leijten FS, Huiskamp G, et al. HFO study group. High frequency oscillations in the intraoperative ECoG to guide epilepsy surgery (‘The HFO Trial’): study protocol for a randomized controlled trial. Trials. 2015;16:422. PubMed PMC
Phase-Amplitude Coupling Localizes Pathologic Brain with Aid of Behavioral Staging in Sleep
High frequency oscillations in epileptic and non-epileptic human hippocampus during a cognitive task
Multicenter intracranial EEG dataset for classification of graphoelements and artifactual signals
Multi-feature localization of epileptic foci from interictal, intracranial EEG
Physiological and pathological high frequency oscillations in focal epilepsy
Lacosamide and Levetiracetam Have No Effect on Sharp-Wave Ripple Rate