High-frequency oscillations of ictal muscle activity and epileptogenic discharges on intracranial EEG in a temporal lobe epilepsy patient

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Abstract

Objective

During seizures, intracranial EEG electrodes can record ictal muscle movements. Our purpose was to differentiate the high-frequency oscillations (HFOs) of extracranial muscle contractions from those of intracranial epileptogenic discharges.

Methods

Using intracranial video-EEG (IVEEG), we recorded seizures in a 17-year-old boy with left mesial–temporal lobe epilepsy. We used multiple band frequency analysis (MBFA) to differentiate extracranial HFOs of craniofacial muscle activities from intracranial HFOs recorded ictally and interictally.

Results

During 11 seizures, IVEEG showed low-amplitude fast waves (∼60 Hz) starting at the left mesial–temporal electrodes. Ictal facial grimacing projected low-amplitude (∼20 μV) fast waves (∼160 Hz) on inferior lateral–temporal electrodes. Interictal chewing projected medium-amplitude (∼100 μV) fast waves (∼140 Hz) correlating to mouth movements. MBFA topographic power spectrograms revealed a sustained, consistent ictal fast-frequency band from electrodes in the seizure-onset zone and randomly scattered HFOs without a specific frequency band from ictal and interictal extracranial muscle contractions.

Conclusions

MBFA power spectrograms differentiated randomly scattered muscle HFOs without a specific frequency band at electrodes close to temporal muscles from ictal epileptic HFOs with a sustained, fast-frequency band in the seizure-onset zone.

Significance

The pattern and distribution of frequency power spectrograms of extracranial HFOs differ from those of intracranial HFOs.

Introduction

When recording clinical seizures, scalp EEG electrodes inevitably capture muscle movements, such as the craniofacial contractions caused by facial grimacing, tongue biting, and mouthing. Injecting botulinum toxin type-A can eliminate electromyography (EMG)-related influences and improve localization and lateralization of intracranial seizure foci during scalp EEG (Eisenschenk et al., 2002). Intracranial EEG electrodes can also record ictal muscle movements. During intracranial EEG recordings, differentiating the discharges derived from muscle from those associated with brain activity is important for localization of epileptogenic discharges.

High-frequency oscillations (HFOs) in the brain can be physiologic or epileptic (Le Van Quyen et al., 2006). Physiologic HFOs include cognitive gamma oscillations of 30–70 Hz (Rodriguez et al., 1999), 200 Hz frequency in the visual cortex (Lachaux et al., 2005), and ripple activity [140–200 Hz] (Staba et al., 2002). Early reports of ictal HFOs documented only frequencies of up to 150 Hz during neocortical partial seizures (Fisher et al., 1992); however, improvements in sampling rate and data storage now allow frequencies of up to 500 Hz to be recorded from intracerebral macroelectrodes (Jirsch et al., 2006, Urrestarazu et al., 2007).

Since ictal HFOs indicate areas of epileptogenesis, distinguishing extracranial nonepileptogenic HFOs from intracranial epileptogenic HFOs would facilitate localization of seizure foci. However, we know little about how muscle impulses reach intracranial EEG electrodes. No prior reports have characterized the HFOs from muscle contractions.

Among frequency analysis methods, such as fast Fourier transform and wavelet transform, multiple band frequency analysis (MBFA) was developed to analyze the characteristics of spectral density during short periods of visual evoked potentials (Shimoyama et al., 2000). MBFA separates a signal into multiple sub-band signal components by multiple band-pass filters.

Previously, we applied MBFA to reveal the spatio-temporal changes of ictal HFOs recorded from intracranial EEG electrodes during neocortical seizures (Akiyama et al., 2005, Akiyama et al., 2006, Ochi et al., 2007). In this report, we utilized MBFA to differentiate the epileptogenic HFOs from extracranial muscle HFOs detected at intracranial electrodes.

This report is the first to characterize the extracranial HFOs of craniofacial muscle movements recorded ictally and interictally in an adolescent boy with mesial–temporal lobe epilepsy.

Section snippets

Patient

We report on a 17-year-old right-handed boy (weight, 83.1 kg; height, 175.5 cm) who had intractable temporal lobe epilepsy secondary to a left mesial–temporal tumor since nine years of age. Initial seizures consisted of ictal laughter with peri-oral cyanosis without aura. He had undergone lesionectomy and multiple subpial transections of the lateral temporal cortex at 11 years. Sixteen months after the first surgery seizures recurred. These seizures consisted of a rising abdominal sensation,

Discussion

Three characteristics differentiated the extracranial and intracranial HFOs in this patient: (1) MBFA power spectrograms of ictal extracranial muscle activity demonstrated randomly scattered HFOs without a specific frequency band, while ictal epileptogenic HFOs had a sustained frequency band; (2) the pattern and distribution of ictal muscle HFOs were identical to the pattern and distribution of the interictal muscle HFOs associated with chewing; (3) ictal muscle HFOs remained in one region

Acknowledgements

We thank Drs. Derrick Chan, Ichiro Sugiyama, Zulma Tovar-Spinoza, Jean Gotman, and Hiroshi Shibasaki for their scientific advice and Ms. Carol L. Squires, Ms. Fatima Ledo, and Ms. Momoko Sugiyama for their editorial assistance.

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