High‐frequency oscillations are not better biomarkers of epileptogenic tissues than spikes

High‐frequency oscillations (HFOs) in intracerebral EEG (stereoelectroencephalography; SEEG) are considered as better biomarkers of epileptogenic tissues than spikes. How this can be applied at the patient level remains poorly understood. We investigated how well HFOs and spikes can predict epileptogenic regions with a large spatial sampling at the patient level.

[1]  H. Lüders,et al.  The epileptogenic zone: general principles. , 2006, Epileptic disorders : international epilepsy journal with videotape.

[2]  A. Wyler Surgery in Epilepsy , 1969, Journal of the Tennessee Medical Association.

[3]  Tommaso Fedele,et al.  Automatic detection of high frequency oscillations during epilepsy surgery predicts seizure outcome , 2016, Clinical Neurophysiology.

[4]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[5]  Jean Gotman,et al.  Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. , 2007, Brain : a journal of neurology.

[6]  Fabrice Wendling,et al.  Defining epileptogenic networks: Contribution of SEEG and signal analysis , 2017, Epilepsia.

[7]  Philip Grewe,et al.  Trends in epilepsy surgery: stable surgical numbers despite increasing presurgical volumes , 2016, Journal of Neurology, Neurosurgery & Psychiatry.

[8]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[9]  B. Brinkmann,et al.  Pathological and physiological high-frequency oscillations in focal human epilepsy. , 2013, Journal of neurophysiology.

[10]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.

[11]  Philippe Kahane,et al.  The temporopolar cortex plays a pivotal role in temporal lobe seizures. , 2005, Brain : a journal of neurology.

[12]  Matt Stead,et al.  Network oscillations modulate interictal epileptiform spike rate during human memory. , 2013, Brain : a journal of neurology.

[13]  Jean Gotman,et al.  Improving the identification of High Frequency Oscillations , 2009, Clinical Neurophysiology.

[14]  J. Gotman,et al.  High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. , 2009, Brain : a journal of neurology.

[15]  C. Bénar,et al.  Pitfalls of high-pass filtering for detecting epileptic oscillations: A technical note on “false” ripples , 2010, Clinical Neurophysiology.

[16]  G. Mathern,et al.  Removing interictal fast ripples on electrocorticography linked with seizure freedom in children , 2010, Neurology.

[17]  Gregory K. Bergey,et al.  Identification of seizure onset zone and preictal state based on characteristics of high frequency oscillations , 2015, Clinical Neurophysiology.

[18]  Jean Gotman,et al.  Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high‐frequency oscillations (80–500 Hz) , 2016, Epilepsia.

[19]  S. Medina Villalon,et al.  EpiTools, A software suite for presurgical brain mapping in epilepsy: Intracerebral EEG , 2018, Journal of Neuroscience Methods.

[20]  Angela Marchi,et al.  Occipital and occipital “plus” epilepsies: A study of involved epileptogenic networks through SEEG quantification , 2016, Epilepsy & Behavior.

[21]  J. Martinerie,et al.  Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. , 2010, Brain : a journal of neurology.

[22]  Shuang Wang,et al.  Ripple classification helps to localize the seizure‐onset zone in neocortical epilepsy , 2013, Epilepsia.

[23]  Jeffery A. Hall,et al.  Interictal high‐frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain , 2008, Epilepsia.

[24]  Hitten P. Zaveri,et al.  The spatial and signal characteristics of physiologic high frequency oscillations , 2014, Epilepsia.

[25]  J. Talairach,et al.  Lesion, "irritative" zone and epileptogenic focus. , 1966, Confinia neurologica.

[26]  Andreas Schulze-Bonhage,et al.  Physiological Ripples Associated with Sleep Spindles Differ in Waveform Morphology from Epileptic Ripples , 2017, Int. J. Neural Syst..

[27]  J. Sarnthein,et al.  Human Intracranial High Frequency Oscillations (HFOs) Detected by Automatic Time-Frequency Analysis , 2014, PloS one.

[28]  Andriy I. Bandos,et al.  On the use of partial area under the ROC curve for comparison of two diagnostic tests , 2015, Biometrical journal. Biometrische Zeitschrift.

[29]  B. Colombet,et al.  AnyWave: A cross-platform and modular software for visualizing and processing electrophysiological signals , 2015, Journal of Neuroscience Methods.

[30]  G. Buzsáki,et al.  tFast Network Oscillations in the Hippocampal CA1 Region of the Behaving Rat , 1999, The Journal of Neuroscience.

[31]  Fabrice Wendling,et al.  Local and remote epileptogenicity in focal cortical dysplasias and neurodevelopmental tumours. , 2009, Brain : a journal of neurology.

[32]  F. Bartolomei,et al.  Visual and semiautomated evaluation of epileptogenicity in focal cortical dysplasias — An intracranial EEG study , 2016, Epilepsy & Behavior.

[33]  John C. Mosher,et al.  Time-Frequency Strategies for Increasing High-Frequency Oscillation Detectability in Intracerebral EEG , 2016, IEEE Transactions on Biomedical Engineering.

[34]  Tom Fawcett,et al.  An introduction to ROC analysis , 2006, Pattern Recognit. Lett..

[35]  Liset Menendez de la Prida,et al.  Conundrums of High-Frequency Oscillations (80–800 Hz) in the Epileptic Brain , 2015, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[36]  Fabrice Wendling,et al.  What is the concordance between the seizure onset zone and the irritative zone? A SEEG quantified study , 2016, Clinical Neurophysiology.

[37]  Philippe Kahane,et al.  Imaging the seizure onset zone with stereo-electroencephalography. , 2011, Brain : a journal of neurology.

[38]  Michel Le Van Quyen,et al.  RIPPLELAB: A Comprehensive Application for the Detection, Analysis and Classification of High Frequency Oscillations in Electroencephalographic Signals , 2016, PloS one.

[39]  D. Louis Collins,et al.  High‐frequency oscillations, extent of surgical resection, and surgical outcome in drug‐resistant focal epilepsy , 2013, Epilepsia.

[40]  Fabrice Wendling,et al.  From mesial temporal lobe to temporoperisylvian seizures: A quantified study of temporal lobe seizure networks , 2010, Epilepsia.

[41]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[42]  P. Chauvel,et al.  Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. , 2008, Brain : a journal of neurology.

[43]  Jean Gotman,et al.  High Frequency Oscillations and spikes: Separating real HFOs from false oscillations , 2016, Clinical Neurophysiology.

[44]  Philippe Kahane,et al.  Temporal lobe epilepsy and hippocampal sclerosis: Lessons from depth EEG recordings , 2010, Epilepsia.

[45]  Fabrice Wendling,et al.  What are the assets and weaknesses of HFO detectors? A benchmark framework based on realistic simulations , 2017, PloS one.

[46]  Martine Gavaret,et al.  Despiking SEEG signals reveals dynamics of gamma band preictal activity , 2017, Physiological measurement.

[47]  Maeike Zijlmans,et al.  Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome , 2015, Neurology.

[48]  Yahya Aghakhani,et al.  Interrater reliability of visually evaluated high frequency oscillations , 2017, Clinical Neurophysiology.

[49]  Philippe Kahane,et al.  Definition and localization of the epileptogenic zone The Bancaud and Talairach view on the epileptogenic zone : a working hypothesis , 2006 .