Journal of Pediatric Epilepsy 2015; 04(04): 156-164
DOI: 10.1055/s-0035-1563729
Review Article
Georg Thieme Verlag KG Stuttgart • New York

High-Frequency Oscillations in Pediatric Epilepsy: Methodology and Clinical Application

Jing Xiang
1   Division of Neurology, MEG Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
,
Kimberly Leiken
1   Division of Neurology, MEG Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
,
Lu Tang
2   Department of Neurology, Nanjing Brain Hospital, Nanjing, People's Republic of China
,
Ailiang Miao
2   Department of Neurology, Nanjing Brain Hospital, Nanjing, People's Republic of China
,
Xiaoshan Wang
2   Department of Neurology, Nanjing Brain Hospital, Nanjing, People's Republic of China
,
Hui Qiao
3   MEG Laboratory, Tiantan Hospital, Beijing, People's Republic of China
,
Bo Sun
3   MEG Laboratory, Tiantan Hospital, Beijing, People's Republic of China
,
Yigang Feng
4   Medical Imaging Center, Guangdong 999 Brain Hospital, Guangzhou, People's Republic of China
,
Milena Korostenskaja
5   Milena's Functional Brain Mapping and Brain Computer Interface Lab, Florida Hospital for Children, Orlando, Florida, United States
6   MEG Lab, Florida Hospital for Children, Orlando, Florida, United States
7   Comprehensive Epilepsy Center, Florida Hospital for Children, Orlando, Florida, United States
› Author Affiliations
Further Information

Publication History

28 August 2014

31 March 2015

Publication Date:
11 September 2015 (online)

Abstract

Increasing evidence indicates that the brain generates signals in a wide-frequency range, including high-frequency brain signals. High-frequency brain signals are also called high-frequency oscillations (HFOs), ripples, or fast ripples. There are no established terms for describing HFOs in a variety of frequency ranges. HFOs are clinically important because early detection of epileptic (or pathologic) high-frequency brain signals may significantly change the clinical management of epilepsy, including pediatric epilepsy. In this article, we review the cerebral mechanisms of HFOs and the maturational changes of HFOs in the developing brain. Newly developed methods for the detection and localization of HFOs are discussed. We describe many recent findings in the literature from invasive electrocorticography recordings, scalp electroencephalography, and magnetoencephalography. We also discuss the clinical importance of HFOs as markers of epileptogenicity and their application in different types of epilepsies. As successful surgical treatment in medically refractory epilepsies largely depends on the identification of epileptogenic zones, the use of HFOs may significantly improve surgical outcomes. Indeed, the removal of brain tissue generating pathological high-frequency signals has been related to better postsurgical outcomes than removal of the seizure onset zones. This indicates that HFOs may mark cortex that needs to be removed to achieve seizure control. The link between the epileptogenic zone and HFOs suggests that their study can elucidate the pathophysiology of epileptogenesis and ictogenesis. In addition, HFOs may reflect the predisposition of the tissue to generate seizures. Finally, we discuss how HFOs can be used to study childhood absence epilepsy, which can only be studied noninvasively.

 
  • References

  • 1 Kerber K, Dümpelmann M, Schelter B , et al. Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures. Clin Neurophysiol 2014; 125 (7) 1339-1345
  • 2 Jobst BC. Are HFOs still UFOs? The known and unknown about high frequency oscillations in epilepsy surgery. Epilepsy Curr 2013; 13 (6) 273-275
  • 3 Bragin A, Engel Jr J, Staba RJ. High-frequency oscillations in epileptic brain. Curr Opin Neurol 2010; 23 (2) 151-156
  • 4 Bragin A, Wilson CL, Almajano J, Mody I, Engel Jr J. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 2004; 45 (9) 1017-1023
  • 5 Engel Jr J, Bragin A, Staba R, Mody I. High-frequency oscillations: what is normal and what is not?. Epilepsia 2009; 50 (4) 598-604
  • 6 Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomarkers Med 2011; 5 (5) 557-566
  • 7 Xiang J, Liu Y, Wang Y , et al. Neuromagnetic correlates of developmental changes in endogenous high-frequency brain oscillations in children: a wavelet-based beamformer study. Brain Res 2009; 1274: 28-39
  • 8 Engel Jr J, da Silva FL. High-frequency oscillations - where we are and where we need to go. Prog Neurobiol 2012; 98 (3) 316-318
  • 9 Jacobs J, Zelmann R, Jirsch J, Chander R, Dubeau CE, Gotman J. High frequency oscillations (80-500 Hz) in the preictal period in patients with focal seizures. Epilepsia 2009; 50 (7) 1780-1792
  • 10 Zijlmans M, Jacobs J, Zelmann R, Dubeau F, Gotman J. High frequency oscillations and seizure frequency in patients with focal epilepsy. Epilepsy Res 2009; 85 (2–3) 287-292
  • 11 Gotman J. High frequency oscillations: the new EEG frontier?. Epilepsia 2010; 51 (Suppl. 01) 63-65
  • 12 Shiraishi H, Haginoya K, Nakagawa E , et al. Magnetoencephalography localizing spike sources of atypical benign partial epilepsy. Brain Dev 2014; 36 (1) 21-27
  • 13 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 (5) 848-857
  • 14 von Ellenrieder N, Beltrachini L, Perucca P, Gotman J. Size of cortical generators of epileptic interictal events and visibility on scalp EEG. Neuroimage 2014; 94: 47-54
  • 15 Jacobs J, Staba R, Asano E , et al. High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol 2012; 98 (3) 302-315
  • 16 Wood H. High-frequency oscillations pinpoint the seizure-onset zone. Nat Rev Neurol 2011; 7 (9) 475
  • 17 Usui N, Terada K, Baba K , et al. Clinical significance of ictal high frequency oscillations in medial temporal lobe epilepsy. Clin Neurophysiol 2011; 122 (9) 1693-1700
  • 18 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 (11) 2212-2219
  • 19 Burnos S, Hilfiker P, Sürücü O , et al. Human intracranial high frequency oscillations (HFOs) detected by automatic time-frequency analysis. PLoS ONE 2014; 9 (4) e94381
  • 20 Zelmann R, Lina JM, Schulze-Bonhage A, Gotman J, Jacobs J. Scalp EEG is not a blur: it can see high frequency oscillations although their generators are small. Brain Topogr 2014; 27 (5) 683-704
  • 21 Xiang J, Luo Q, Kotecha R , et al. Accumulated source imaging of brain activity with both low and high-frequency neuromagnetic signals. Front Neuroinform 2014; 8 (57) 57
  • 22 Miao A, Xiang J, Tang L , et al. Using ictal high-frequency oscillations (80-500Hz) to localize seizure onset zones in childhood absence epilepsy: a MEG study. Neurosci Lett 2014; 566: 21-26
  • 23 Miao A, Tang L, Xiang J , et al. Dynamic magnetic source imaging of absence seizure initialization and propagation: a magnetoencephalography study. Epilepsy Res 2014; 108 (3) 468-480
  • 24 Xiang J, Holowka S, Qiao H , et al. Automatic localization of epileptic zones using magnetoencephalography. Neurol Clin Neurophysiol 2004; 2004 (4) 98
  • 25 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 (3) 301-310
  • 26 Dzhala VI, Staley KJ. Mechanisms of fast ripples in the hippocampus. J Neurosci 2004; 24 (40) 8896-8906
  • 27 Simeone TA, Samson KK, Matthews SA, Simeone KA. In vivo ketogenic diet treatment attenuates pathologic sharp waves and high frequency oscillations in in vitro hippocampal slices from epileptic Kv 1.1α knockout mice. Epilepsia 2014; 55 (5) e44-e49
  • 28 Cid E, Gomez-Dominguez D, Martin-Lopez D , et al. Dampened hippocampal oscillations and enhanced spindle activity in an asymptomatic model of developmental cortical malformations. Front Syst Neurosci 2014; 8: 50
  • 29 Aivar P, Valero M, Bellistri E, Menendez de la Prida L. Extracellular calcium controls the expression of two different forms of ripple-like hippocampal oscillations. J Neurosci 2014; 34 (8) 2989-3004
  • 30 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 (6) 930-941
  • 31 Staley KJ. Neurons skip a beat during fast ripples. Neuron 2007; 55 (6) 828-830
  • 32 Pearce A, Wulsin D, Blanco JA, Krieger A, Litt B, Stacey WC. Temporal changes of neocortical high-frequency oscillations in epilepsy. J Neurophysiol 2013; 110 (5) 1167-1179
  • 33 Ventura-Mejía C, Medina-Ceja L. Decreased fast ripples in the hippocampus of rats with spontaneous recurrent seizures treated with carbenoxolone and quinine. Biomed Res Int 2014; 2014: 282490
  • 34 Köhling R, Staley K. Network mechanisms for fast ripple activity in epileptic tissue. Epilepsy Res 2011; 97 (3) 318-323
  • 35 Xiang J, Wang Y, Chen Y , et al. Noninvasive localization of epileptogenic zones with ictal high-frequency neuromagnetic signals. J Neurosurg Pediatr 2010; 5 (1) 113-122
  • 36 Le Van Quyen M, Khalilov I, Ben-Ari Y. The dark side of high-frequency oscillations in the developing brain. Trends Neurosci 2006; 29 (7) 419-427
  • 37 Zhang ZJ, Valiante TA, Carlen PL. Transition to seizure: from “macro”- to “micro”-mysteries. Epilepsy Res 2011; 97 (3) 290-299
  • 38 Hamzei-Sichani F, Davidson KG, Yasumura T , et al. Mixed electrical-chemical synapses in adult rat hippocampus are primarily glutamatergic and coupled by Connexin-36. Front Neuroanat 2012; 6: 13
  • 39 Hamzei-Sichani F, Kamasawa N, Janssen WG , et al. Gap junctions on hippocampal mossy fiber axons demonstrated by thin-section electron microscopy and freeze fracture replica immunogold labeling. Proc Natl Acad Sci U S A 2007; 104 (30) 12548-12553
  • 40 Khalilov I, Le Van Quyen M, Gozlan H, Ben-Ari Y. Epileptogenic actions of GABA and fast oscillations in the developing hippocampus. Neuron 2005; 48 (5) 787-796
  • 41 Traub RD, Bibbig A. A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J Neurosci 2000; 20 (6) 2086-2093
  • 42 Cooper R, Winter AL, Crow HJ, Walter WG. Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man. Electroencephalogr Clin Neurophysiol 1965; 18: 217-228
  • 43 Murakami S, Zhang T, Hirose A, Okada YC. Physiological origins of evoked magnetic fields and extracellular field potentials produced by guinea-pig CA3 hippocampal slices. J Physiol 2002; 544 (Pt 1) 237-251
  • 44 Le Van Quyen M, Bragin A, Staba R, Crépon B, Wilson CL, Engel Jr J. Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J Neurosci 2008; 28 (24) 6104-6110
  • 45 Frei MG, Zaveri HP, Arthurs S , et al. Controversies in epilepsy: debates held during the Fourth International Workshop on Seizure Prediction. Epilepsy Behav 2010; 19 (1) 4-16
  • 46 Amor F, Baillet S, Navarro V, Adam C, Martinerie J, Quyen MleV. Cortical local and long-range synchronization interplay in human absence seizure initiation. Neuroimage 2009; 45 (3) 950-962
  • 47 Martinerie J, Adam C, Le Van Quyen M , et al. Epileptic seizures can be anticipated by non-linear analysis. Nat Med 1998; 4 (10) 1173-1176
  • 48 Mari F, Zelmann R, Andrade-Valenca L, Dubeau F, Gotman J. Continuous high-frequency activity in mesial temporal lobe structures. Epilepsia 2012; 53 (5) 797-806
  • 49 Zelmann R, Mari F, Jacobs J, Zijlmans M, Dubeau F, Gotman J. A comparison between detectors of high frequency oscillations. Clin Neurophysiol 2012; 123 (1) 106-116
  • 50 Salami P, Lévesque M, Gotman J, Avoli M. A comparison between automated detection methods of high-frequency oscillations (80-500 Hz) during seizures. J Neurosci Methods 2012; 211 (2) 265-271
  • 51 Kobayashi K, Agari T, Oka M , et al. Detection of seizure-associated high-frequency oscillations above 500Hz. Epilepsy Res 2010; 88 (2–3) 139-144
  • 52 Makeyev O, Liu X, Wang L , et al. Feasibility of recording high frequency oscillations with tripolar concentric ring electrodes during pentylenetetrazole-induced seizures in rats. Conf Proc IEEE Eng Med Biol Soc 2012; 2012 (12) 4599-4602
  • 53 Staba RJ, Wilson CL, Bragin A, Fried I, Engel Jr J. Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 2002; 88 (4) 1743-1752
  • 54 Xiang J, Liu Y, Wang Y , et al. Frequency and spatial characteristics of high-frequency neuromagnetic signals in childhood epilepsy. Epileptic Disord 2009; 11 (2) 113-125
  • 55 Zijlmans M, Jiruska P, Zelmann R, Leijten FS, Jefferys JG, Gotman J. High-frequency oscillations as a new biomarker in epilepsy. Ann Neurol 2012; 71 (2) 169-178
  • 56 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 (2) 286-296
  • 57 Zelmann R, Zijlmans M, Jacobs J, Châtillon CE, Gotman J. Improving the identification of High Frequency Oscillations. Clin Neurophysiol 2009; 120 (8) 1457-1464
  • 58 Gloss D, Nolan SJ, Staba R. The role of high-frequency oscillations in epilepsy surgery planning. Cochrane Database Syst Rev 2014; 1: CD010235
  • 59 Srejic LR, Valiante TA, Aarts MM, Hutchison WD. High-frequency cortical activity associated with postischemic epileptiform discharges in an in vivo rat focal stroke model. J Neurosurg 2013; 118 (5) 1098-1106
  • 60 Kalitzin S, Zijlmans M, Petkov G , et al. Quantification of spontaneous and evoked HFO's in SEEG recording and prospective for pre-surgical diagnostics. Case study. Conf Proc IEEE Eng Med Biol Soc 2012; 2012 (12) 1024-1027
  • 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 (Pt 9) 2354-2366
  • 62 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 (11) 2130-2138
  • 63 Bragin A, Mody I, Wilson CL, Engel Jr J. Local generation of fast ripples in epileptic brain. J Neurosci 2002; 22 (5) 2012-2021
  • 64 Bragin A, Wilson CL, Staba RJ, Reddick M, Fried I, Engel Jr J. Interictal high-frequency oscillations (80-500 Hz) in the human epileptic brain: entorhinal cortex. Ann Neurol 2002; 52 (4) 407-415
  • 65 Bragin A, Engel Jr J, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus 1999; 9 (2) 137-142
  • 66 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 2009; 50 (4) 605-616
  • 67 Bagshaw AP, Jacobs J, LeVan P, Dubeau F, Gotman J. Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy. Epilepsia 2009; 50 (4) 617-628
  • 68 Brázdil M, Halámek J, Jurák P , et al. Interictal high-frequency oscillations indicate seizure onset zone in patients with focal cortical dysplasia. Epilepsy Res 2010; 90 (1–2) 28-32
  • 69 Jacobs J, Levan P, Châtillon CE, Olivier A, Dubeau F, Gotman J. High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. Brain 2009; 132 (Pt 4) 1022-1037
  • 70 Jirsch JD, Urrestarazu E, LeVan P, Olivier A, Dubeau F, Gotman J. High-frequency oscillations during human focal seizures. Brain 2006; 129 (Pt 6) 1593-1608
  • 71 Pfurtscheller G, Cooper R. Frequency dependence of the transmission of the EEG from cortex to scalp. Electroencephalogr Clin Neurophysiol 1975; 38 (1) 93-96
  • 72 Whitham EM, Pope KJ, Fitzgibbon SP , et al. Scalp electrical recording during paralysis: quantitative evidence that EEG frequencies above 20 Hz are contaminated by EMG. Clin Neurophysiol 2007; 118 (8) 1877-1888
  • 73 Kobayashi K, Yoshinaga H, Toda Y, Inoue T, Oka M, Ohtsuka Y. High-frequency oscillations in idiopathic partial epilepsy of childhood. Epilepsia 2011; 52 (10) 1812-1819
  • 74 Wu JY, Koh S, Sankar R, Mathern GW. Paroxysmal fast activity: an interictal scalp EEG marker of epileptogenesis in children. Epilepsy Res 2008; 82 (1) 99-106
  • 75 Kobayashi K, Ohmori I, Hayashi K , et al. High-frequency EEG oscillations in hyperthermia-induced seizures of Scn1a mutant rats. Epilepsy Res 2013; 103 (2–3) 161-166
  • 76 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 2010; 51 (10) 2190-2194
  • 77 Andrade-Valença L, Mari F, Jacobs J , et al. Interictal high frequency oscillations (HFOs) in patients with focal epilepsy and normal MRI. Clin Neurophysiol 2012; 123 (1) 100-105
  • 78 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 (3) 345-356
  • 79 Rampp S, Kaltenhäuser M, Weigel D , et al. MEG correlates of epileptic high gamma oscillations in invasive EEG. Epilepsia 2010; 51 (8) 1638-1642
  • 80 Guggisberg AG, Kirsch HE, Mantle MM, Barbaro NM, Nagarajan SS. Fast oscillations associated with interictal spikes localize the epileptogenic zone in patients with partial epilepsy. Neuroimage 2008; 39 (2) 661-668
  • 81 Staba RJ, Wilson CL, Bragin A, Jhung D, Fried I, Engel Jr J. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann Neurol 2004; 56 (1) 108-115
  • 82 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 (9) 1607-1617
  • 83 König MW, Mahmoud MA, Fujiwara H, Hemasilpin N, Lee KH, Rose DF. Influence of anesthetic management on quality of magnetoencephalography scan data in pediatric patients: a case series. Paediatr Anaesth 2009; 19 (5) 507-512