Detection of High-Frequency Oscillations by Hybrid Depth Electrodes in Standard Clinical Intracranial EEG Recordings

High-frequency oscillations (HFOs) have been proposed as a novel marker for epileptogenic tissue, spurring tremendous research interest into the characterization of these transient events. A wealth of continuously recorded intracranial electroencephalographic (iEEG) data is currently available from patients undergoing invasive monitoring for the surgical treatment of epilepsy. In contrast to data recorded on research-customized recording systems, data from clinical acquisition systems remain an underutilized resource for HFO detection in most centers. The effective and reliable use of this clinically obtained data would be an important advance in the ongoing study of HFOs and their relationship to ictogenesis. The diagnostic utility of HFOs ultimately will be limited by the ability of clinicians to detect these brief, sporadic, and low amplitude events in an electrically noisy clinical environment. Indeed, one of the most significant factors limiting the use of such clinical recordings for research purposes is their low signal to noise ratio, especially in the higher frequency bands. In order to investigate the presence of HFOs in clinical data, we first obtained continuous intracranial recordings in a typical clinical environment using a commercially available, commonly utilized data acquisition system and “off the shelf” hybrid macro-/micro-depth electrodes. These data were then inspected for the presence of HFOs using semi-automated methods and expert manual review. With targeted removal of noise frequency content, HFOs were detected on both macro- and micro-contacts, and preferentially localized to seizure onset zones. HFOs detected by the offline, semi-automated method were also validated in the clinical viewer, demonstrating that (1) this clinical system allows for the visualization of HFOs and (2) with effective signal processing, clinical recordings can yield valuable information for offline analysis.

[1]  Guglielmo Foffani,et al.  Reduced Spike-Timing Reliability Correlates with the Emergence of Fast Ripples in the Rat Epileptic Hippocampus , 2007, Neuron.

[2]  Itzhak Fried,et al.  Increased Fast ripple to ripple Ratios Correlate with Reduced Hippocampal Volumes and Neuron Loss in Temporal Lobe Epilepsy Patients , 2007, Epilepsia.

[3]  Regula S Briellmann,et al.  Temporal lobectomy: long-term seizure outcome, late recurrence and risks for seizure recurrence. , 2004, Brain : a journal of neurology.

[4]  M. Steriade,et al.  Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. , 2001, Journal of neurophysiology.

[5]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[6]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[7]  Spencer Kellis,et al.  Potential for unreliable interpretation of EEG recorded with microelectrodes , 2013, Epilepsia.

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

[9]  Ayako Ochi,et al.  Dynamic Changes of Ictal High‐Frequency Oscillations in Neocortical Epilepsy: Using Multiple Band Frequency Analysis , 2007, Epilepsia.

[10]  Charles L. Wilson,et al.  High‐frequency Oscillations after Status Epilepticus: Epileptogenesis and Seizure Genesis , 2004, Epilepsia.

[11]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[12]  Jerome Engel,et al.  High-frequency oscillations in epileptic brain , 2010, Current opinion in neurology.

[13]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Menno Witter Entorhinal cortex , 2011, Scholarpedia.

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

[16]  J. Jefferys,et al.  High‐frequency oscillations as a new biomarker in epilepsy , 2012, Annals of neurology.

[17]  Itzhak Fried,et al.  Interictal high‐frequency oscillations (80–500Hz) in the human epileptic brain: Entorhinal cortex , 2002, Annals of neurology.

[18]  J. Fell,et al.  Ripples in the medial temporal lobe are relevant for human memory consolidation. , 2008, Brain : a journal of neurology.

[19]  J. Gotman,et al.  Influence of contact size on the detection of HFOs in human intracerebral EEG recordings , 2013, Clinical Neurophysiology.

[20]  Fabrice Wendling,et al.  Mechanisms of physiological and epileptic HFO generation , 2012, Progress in Neurobiology.

[21]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[22]  Brian Litt,et al.  Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings , 2007, Clinical Neurophysiology.

[23]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[24]  György Buzsáki,et al.  High frequency oscillations in the intact brain , 2012, Progress in Neurobiology.

[25]  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.