Localizing epileptogenic regions using high-frequency oscillations and machine learning.

HFO; artificial intelligence; epilepsy; epilepsy surgery; epileptiform spike; fast ripple; high-frequency oscillation; machine learning; phase-amplitude coupling; ripple; seizure; wavelet

Abstract :

[en] Pathological high frequency oscillations (HFOs) are putative neurophysiological biomarkers of epileptogenic brain tissue. Utilizing HFOs for epilepsy surgery planning offers the promise of improved seizure outcomes for patients with medically refractory epilepsy. This review discusses possible machine learning strategies that can be applied to HFO biomarkers to better identify epileptogenic regions. We discuss the role of HFO rate, and utilizing features such as explicit HFO properties (spectral content, duration, and power) and phase-amplitude coupling for distinguishing pathological HFO (pHFO) events from physiological HFO events. In addition, the review highlights the importance of neuroanatomical localization in machine learning strategies.

Disciplines :

Neurology

Author, co-author :

Weiss, Shennan A.

Waldman, Zachary

Raimondo, Federico ; Université de Liège - ULiège > Consciousness-Coma Science Group

Slezak, Diego

Donmez, Mustafa

Worrell, Gregory

Bragin, Anatol

Engel, Jerome

Staba, Richard

Sperling, Michael

Language :

English

Title :

Localizing epileptogenic regions using high-frequency oscillations and machine learning.

Publication date :

2019

Journal title :

Biomarkers in Medicine

ISSN :

1752-0363

eISSN :

1752-0371

Publisher :

Future Medicine, London, United Kingdom

Volume :

Issue :

Pages :

409-418

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 17 January 2020

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Bibliography

Vakharia VN, Duncan JS, Witt J-A, Elger CE, Staba R, Engel J. Getting the best outcomes from epilepsy surgery. Ann. Neurol. 83(4), 676-690 (2018).
Weiss SA, Berry B, Chervoneva I et al. Visually validated semi-automatic high-frequency oscillation detection aides the delineation of epileptogenic regions during intra-operative electrocorticography. Clin. Neurophysiol. 129(10), 2089-2098 (2018).
van 't Klooster MA, van Klink NEC, Zweiphenning WJEM et al. Tailoring epilepsy surgery with fast ripples in the intraoperative electrocorticogram. Ann. Neurol. 81(5), 664-676 (2017).
van 't Klooster MA, van Klink NEC, Leijten FSS et al. Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome. Neurology 85(2), 120-128 (2015).
LoPinto-Khoury C, Sperling MR, Skidmore C et al. Surgical outcome in PET-positive, MRI-negative patients with temporal lobe epilepsy. Epilepsia 53(2), 342-348 (2012).
Holtkamp M, Sharan A, Sperling MR. Intracranial EEG in predicting surgical outcome in frontal lobe epilepsy. Epilepsia 53(10), 1739-1745 (2012).
Ung H, Davis KA, Wulsin D et al. Temporal behavior of seizures and interictal bursts in prolonged intracranial recordings from epileptic canines. Epilepsia 57(12), 1949-1957 (2016).
King-Stephens D, Mirro E, Weber PB et al. Lateralization of mesial temporal lobe epilepsy with chronic ambulatory electrocorticography. Epilepsia 56(6), 959-967 (2015).
Engel J, Bragin A, Staba R, Mody I. High-frequency oscillations: What is normal and what is not Epilepsia 50(4), 598-604 (2009).
Frauscher B, Bartolomei F, Kobayashi K et al. High-frequency oscillations: The state of clinical research. Epilepsia 58(8), 1316-1329 (2017).
Bragin A, Engel J, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus 9(2), 137-142 (1999).
Staba RJ, Wilson CL, Bragin A, Fried I, Engel J. Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol. 88(4), 1743-1752 (2002).
Staba RJ, Wilson CL, Bragin A, Jhung D, Fried I, Engel J. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann. Neurol. 56(1), 108-115 (2004).
Jacobs J, LeVan P, Chander R, Hall J, Dubeau F, Gotman J. Interictal high-frequency oscillations (80-500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia 49(11), 1893-1907 (2008).
Jacobs J, Zijlmans M, Zelmann R et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann. Neurol. 67(2), 209-220 (2010).
Fedele T, Burnos S, Boran E et al. Resection of high frequency oscillations predicts seizure outcome in the individual patient. Sci. Rep. 7(1), 13836 (2017).
Zijlmans M, Worrell GA, Dümpelmann M et al. How to record high-frequency oscillations in epilepsy: A practical guideline. Epilepsia 58(8), 1305-1315 (2017).
Shimamoto S, Waldman ZJ, Orosz I et al. Utilization of independent component analysis for accurate pathological ripple detection in intracranial EEG recordings recorded extra-A nd intra-operatively. Clin. Neurophysiol. 129(1), 296-307 (2018).
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. 121(3), 301-310 (2010).
Canolty RT, Edwards E, Dalal SS et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313(5793), 1626-1628 (2006).
Frauscher B, von Ellenrieder N, Zelmann R et al. High-frequency oscillations in the normal human brain. Ann. Neurol. 84, 374-385 (2018).
Waldman ZJ, Camarillo-Rodriguez L, Chervenova I et al. Ripple oscillations in the left temporal neocortex are associated with impaired verbal episodic memory encoding. Epilepsy Behav. 88, 33-40 (2018).
Weiss SA, Orosz I, Salamon N et al. Ripples on spikes show increased phase-amplitude coupling in mesial temporal lobe epilepsy seizure-onset zones. Epilepsia 57(11), 1916-1930 (2016).
Song I, Orosz I, Chervoneva I et al. Bimodal coupling of ripples and slower oscillations during sleep in patients with focal epilepsy. Epilepsia 58(11), 1972-1984 (2017).
Staba RJ, Frighetto L, Behnke EJ et al. Increased fast ripple to ripple ratios correlate with reduced hippocampal volumes and neuron loss in temporal lobe epilepsy patients. Epilepsia 48(11), 2130-2138 (2007).
Jacobs J, Levan P, Châtillon C-E, Olivier A, Dubeau F, Gotman J. High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. Brain J. Neurol. 132(Pt 4), 1022-1037 (2009).
Crépon B, Navarro V, HasbounDet al. Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. Brain J. Neurol. 133(Pt 1), 33-45 (2010).
Worrell GA, Gardner AB, Stead SM et al. High-frequency oscillations in human temporal lobe: Simultaneous microwire and clinical macroelectrode recordings. Brain J. Neurol. 131(Pt 4), 928-937 (2008).
Haegelen C, Perucca P, Châtillon C-E et al. High-frequency oscillations, extent of surgical resection, and surgical outcome in drug-resistant focal epilepsy. Epilepsia 54(5), 848-857 (2013).
Roehri N, Pizzo F, Lagarde S et al. High-frequency oscillations are not better biomarkers of epileptogenic tissues than spikes. Ann. Neurol. 83(1), 84-97 (2018).
Jacobs J, Wu JY, Perucca P et al. Removing high-frequency oscillations: A prospective multicenter study on seizure outcome. Neurology 91, 1040-1052 (2018).
Fedele T, van 't Klooster M, Burnos S et al. Automatic detection of high frequency oscillations during epilepsy surgery predicts seizure outcome. Clin. Neurophysiol. 127(9), 3066-3074 (2016).
Wang S, Wang IZ, Bulacio JC et al. Ripple classification helps to localize the seizure-onset zone in neocortical epilepsy. Epilepsia 54(2), 370-376 (2013).
Wang S, So NK, Jin B et al. Interictal ripples nested in epileptiform discharge help to identify the epileptogenic zone in neocortical epilepsy. Clin. Neurophysiol. 128(6), 945-951 (2017).
Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science 256(5059), 1025-1027 (1992).
Buzsáki G. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 25(10), 1073-1188 (2015).
Khodagholy D, Gelinas JN, Buzsáki G. Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus. Science 358(6361), 369-372 (2017).
Jacobs J, Banks S, Zelmann R, Zijlmans M, Jones-Gotman M, Gotman J. Spontaneous ripples in the hippocampus correlate with epileptogenicity and not memory function in patients with refractory epilepsy. Epilepsy Behav. 62, 258-266 (2016).
Guragain H, Cimbalnik J, Stead M et al. Spatial variation in high-frequency oscillation rates and amplitudes in intracranial EEG. Neurology 90(8), e639-e646 (2018).
Alkawadri R, Gaspard N, Goncharova II et al. The spatial and signal characteristics of physiologic high frequency oscillations. Epilepsia 55(12), 1986-1995 (2014).
Waldman ZJ, Shimamoto S, Song I et al. A method for the topographical identification and quantification of high frequency oscillations in intracranial electroencephalography recordings. Clin. Neurophysiol. 129(1), 308-318 (2018).
Pail M, Halámek J, Daniel P et al. Intracerebrally recorded high frequency oscillations: Simple visual assessment versus automated detection. Clin. Neurophysiol. 124(10), 1935-1942 (2013).
Mooij AH, Frauscher B, Amiri M, Otte WM, Gotman J. Differentiating epileptic from non-epileptic high frequency intracerebral EEG signals with measures of wavelet entropy. Clin. Neurophysiol. 127(12), 3529-3536 (2016).
Liu S, Gurses C, Sha Z et al. Stereotyped high-frequency oscillations discriminate seizure onset zones and critical functional cortex in focal epilepsy. Brain J. Neurol. 141, 713-730 (2018).
Liu S, Sha Z, Sencer A et al. Exploring the time-frequency content of high frequency oscillations for automated identification of seizure onset zone in epilepsy. J. Neural Eng. 13(2), 026026 (2016).
Pearce A, Wulsin D, Blanco JA, Krieger A, Litt B, Stacey WC. Temporal changes of neocortical high-frequency oscillations in epilepsy. J. Neurophysiol. 110(5), 1167-1179 (2013).
Blanco JA, Stead M, Krieger A et al. Data mining neocortical high-frequency oscillations in epilepsy and controls. Brain J. Neurol. 134(Pt 10), 2948-2959 (2011).
Pail M, Rehulka P, Cimbálńk J, Dolezalová I, Chrastina J, Brázdil M. Frequency-independent characteristics of high-frequency oscillations in epileptic and non-epileptic regions. Clin. Neurophysiol. 128(1), 106-114 (2017).
Amiri M, Frauscher B, Gotman J. Phase-amplitude coupling is elevated in deep sleep and in the onset zone of focal epileptic seizures. Front Hum. Neurosci. 10, 387 (2016).
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 J. Neurol. 138(Pt 6), 1629-1641 (2015).
Bragin A, Benassi SK, Engel J. Patterns of the UP-DOWN state in normal and epileptic mice. Neuroscience 225, 76-87 (2012).
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 57(6), 869-878 (2016).
Lévesque M, Salami P, Shiri Z, Avoli M. Interictal oscillations and focal epileptic disorders. Eur. J. Neurosci. 48, 2915-2927 (2017).
Khoo HM, von Ellenrieder N, Zazubovits N, He D, Dubeau F, Gotman J. The spike onset zone: The region where epileptic spikes start and from where they propagate. Neurology 91(7), e666-e674 (2018).
Tamilia E, Park E-H, Percivati S et al. Surgical resection of ripple onset predicts outcome in pediatric epilepsy. Ann. Neurol. 84, 331-346 (2018).
Lagarde S, Roehri N, Lambert I et al. Interictal stereotactic-EEG functional connectivity in refractory focal epilepsies. Brain J. Neurol. 141, 2966-2980 (2018).