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Published on: December 18, 2016
Fast ripple analysis in human mesial temporal lobe epilepsy suggests two different seizure-generating mechanisms
Jan Schönberger1, Birgit Frauscher2, Nicolás von Ellenrieder2
1Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal H3A 2B4, QC, Canada; Universitätsklinikum Freiburg, Klinik für Neuropädiatrie und Muskelerkrankungen, Mathildenstraße 1, 79106 Freiburg im Breisgau, Germany; Universitätsklinikum Heidelberg, Zentrum für Kinder- und Jugendmedizin, Klinik Kinderheilkunde I, Sektion für Neuropädiatrie und Stoffwechselmedizin, Im Neuenheimer Feld 430, 69120 Heidelberg, Germany.
Objective:
The distinction of hypersynchronous (HYP) and low-voltage fast (LVF) onset seizures in mesial temporal lobe epilepsy (MTLE) is well established, but classifying individual seizures and patients is often challenging. Experimental work indicates a strong association of HYP with fast ripples (250-500 Hz) and of LVF with ripples (80-250 Hz). We aimed to investigate whether analysis of high-frequency oscillations can be useful for characterizing the process of seizure generation in human MTLE patients.
Methods:
We retrospectively compared 19 HYP and 14 LVF onset clinical seizures from ten and six consecutive MTLE patients with a predominance of the respective pattern. Five-second intervals of stereotactic EEGs from the seizure onset zone were selected, each representing the onset of HYP and LVF, the corresponding pre-ictal periods and, after the large spikes of HYP onsets, the LVF-like pattern that frequently followed.
Results:
Pre-ictal fast ripple density and rate were higher for HYP than for LVF seizures (p < .05). This association was also found for initial ictal segments (p < .001). Furthermore, fast ripple density and rate were higher during the LVF-like pattern after HYP spikes than during LVF without preceding HYP (p < .01). Ripple density and rate in contrast did not differ significantly (p > .05). Fast ripple (p < .01) and ripple (p < .001) amplitude was higher during the LVF-like pattern after HYP spikes when compared to LVF without preceding HYP.
Significance:
Our findings indicate a clear connection between experimental findings and human epilepsy. The association of fast ripples with HYP suggests that out-of-phase firing of different pyramidal cell clusters contributes specifically to generation of these seizures, rather than to LVF onsets. Both during and immediately before seizures, fast ripple analysis may facilitate classification.
Insights
High-frequency oscillations, specifically fast ripples, help distinguish hypersynchronous (HYP) from low-voltage fast (LVF) onset seizures in mesial temporal lobe epilepsy (MTLE). This analysis aids in classifying seizure types and understanding their generation.
Area of Science:
- Neuroscience
- Epileptology
- Computational Neuroscience
Background:
- Distinguishing hypersynchronous (HYP) and low-voltage fast (LVF) onset seizures in mesial temporal lobe epilepsy (MTLE) is crucial but challenging.
- Experimental studies link HYP seizures to fast ripples (250-500 Hz) and LVF seizures to ripples (80-250 Hz).
- Understanding seizure generation mechanisms in MTLE requires precise classification of seizure types.
Purpose of the Study:
- To investigate the utility of high-frequency oscillation (HFO) analysis in characterizing seizure generation processes in human MTLE patients.
- To determine if HFO patterns can aid in differentiating HYP and LVF onset seizures.
Main Methods:
- Retrospective analysis of stereotactic electroencephalograms (EEGs) from 19 HYP and 14 LVF onset seizures in MTLE patients.
- Comparison of pre-ictal and ictal HFO (ripples and fast ripples) density, rate, and amplitude.
- Analysis included seizure onset, pre-ictal periods, and post-HYP spike LVF-like patterns.
Main Results:
- Higher pre-ictal and ictal fast ripple density and rate were observed in HYP seizures compared to LVF seizures.
- Fast ripple density and rate were significantly elevated during LVF-like patterns following HYP spikes.
- Ripple density and rate did not show significant differences between groups, but ripple amplitude was higher in the post-HYP LVF-like pattern.
Conclusions:
- Fast ripple activity is strongly associated with HYP seizure onsets in MTLE, suggesting a role for out-of-phase pyramidal cell firing.
- HFO analysis, particularly of fast ripples, can facilitate the classification of individual seizures and patients during and before seizure onset.
- Findings bridge experimental observations with human epilepsy, offering insights into seizure generation mechanisms.
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