Microseizures and the spatiotemporal scales of human partial epilepsy

Stead, Matt; Bower, Mark R.; Brinkmann, Benjamin H.; Lee, Kendall; Marsh, W. Richard; Meyer, Fredric B.; Litt, Brian; Gompel, Jamie Van; Worrell, Greg

doi:10.1093/brain/awq190

Cited by 283 publications

(272 citation statements)

References 28 publications

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“…These observations suggest the local generation of gamma-IEDs, reminiscent of "microdischarges" that can propagate into widespread epileptiform discharges visible on clinical macroelectrodes. 8 The gamma-IEDs could thus mark the IED source, and illuminate the mechanisms underlying IED generation-a hypothesis that will need to be further investigated.…”

Section: Resultsmentioning

confidence: 99%

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

et al. 2015

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Objective: To investigate the generation, spectral characteristics, and potential clinical significance of brain activity preceding interictal epileptiform spike discharges (IEDs) recorded with intracranial EEG.Methods: Seventeen adult patients with drug-resistant temporal lobe epilepsy were implanted with intracranial electrodes as part of their evaluation for epilepsy surgery. IEDs detected on clinical macro-and research microelectrodes were analyzed using time-frequency spectral analysis.Results: Gamma frequency oscillations (30-100 Hz) often preceded IEDs in spatially confined brain areas. The gamma-IEDs were consistently observed 35 to 190 milliseconds before the epileptiform spike waveforms on individual macro-and microelectrodes. The gamma oscillations associated with IEDs had longer duration (p , 0.001) and slightly higher frequency (p 5 0.045) when recorded on microelectrodes compared with clinical macroelectrodes. Although gammaIEDs comprised only a subset of IEDs, they were strongly associated with electrodes in the seizure onset zone (SOZ) compared with the surrounding brain regions (p 5 0.004), in sharp contrast to IEDs without preceding gamma oscillations that were often also detected outside of the SOZ. Similar to prior studies, isolated pathologic high-frequency oscillations in the gamma (30-100 Hz) and higher (100-600 Hz) frequency range, not associated with an IED, were also found to be associated with SOZ. Conclusions:The occurrence of locally generated gamma oscillations preceding IEDs suggests a mechanistic role for gamma in pathologic network activity generating IEDs. The results show a strong association between SOZ and gamma-IEDs. The potential clinical application of gammaIEDs for mapping pathologic brain regions is intriguing, but will require future prospective studies. Neurology ® 2015;84:602-608 GLOSSARY HFO 5 high-frequency oscillation; IED 5 interictal epileptiform discharge; iEEG 5 intracranial EEG; SOZ 5 seizure onset zone.Interictal epileptiform spike discharges (IEDs) manifest as sharp-wave deflections in the local field potential recorded within the "irritative zone" of epileptic brain.1 The irritative zone is distinct from the seizure onset zone (SOZ), where the ictal discharge is first observed. The relationship between the 2 zones or between IEDs and seizures remains unclear (for review, see de Curtis and Avanzini 2 ). In particular, the processes underlying IED generation are not well understood, and on a cellular level, recordings show a heterogeneous profile of increased, decreased, or unchanged neuronal firing during IEDs.3,4 Furthermore, the spatial extent of IEDs and their association with SOZ has long been recognized to be highly variable. 2Network local field potential oscillations that can be detected with intracranial EEG (iEEG) provide a powerful window into synchronized activity of neuronal populations. Oscillations in the gamma frequency range (30-100 Hz) were recently implicated in the neuronal network generation of ictal-like discharges in an in vitro...

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Section: Resultsmentioning

confidence: 99%

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

et al. 2015

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“…In particular, if ictogenesis is a rather spatially local mechanism in the seizure onset zone, electrode contacts need to be abundant enough to cover a large volume (covering the seizure onset zone) and able to record from small enough volume in order to pick up any preictal change. Such electrode contacts do exist in the form of micro-contacts (Kelly et al, 2007;Stead et al, 2010) and studies on seizure prediction analysing data recorded with these electrodes are expected to provide answers to important questions on seizure predictability.…”

Section: Discussionmentioning

confidence: 99%

Seizure prediction in patients with mesial temporal lobe epilepsy using EEG measures of state similarity

Gadhoumi

Lina

Gotman

2013

Clinical Neurophysiology

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Objectives-In patients with intractable epilepsy, predicting seizures above chance and with clinically acceptable performance has yet to be demonstrated. In this study, an intracranial EEGbased seizure prediction method using measures of similarity with a reference state is proposed.Methods-1565 h of continuous intracranial EEG data from 17 patients with mesial temporal lobe epilepsy were investigated. The recordings included 175 seizures. In each patient the data was split into a training set and a testing set. EEG segments were analyzed using continuous wavelet transform. During training, a reference state was defined in the immediate preictal data and used to derive three features quantifying the discrimination between preictal and interictal states. A classifier was then trained in the feature space. Its performance was assessed using testing set and compared with a random predictor for statistical validation.Results-Better than random prediction performance was achieved in 7 patients. The sensitivity was higher than 85%, the warning rate was less than 0.35/h and the proportion of time under warning was less than 30%.Conclusion-Seizures are predicted above chance in 41% of patients using measures of state similarity.Significance-Sensitivity and specificity levels are potentially interesting for closed-loop seizure control applications.

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“…These functional data are supported by the demonstration that the histopathological damage in mesial TLE cannot be considered "focal," because it includes different hippocampal and parahippocampal structures with variable rostrocaudal extension (Moran et al 2001;Ogren et al 2009;Tassi et al 2010). Finally, intracranial microelectrode recordings in humans have shown that partial seizure may initiate in different areas or microregions within the epileptogenic zone (Stead et al 2010), suggesting that the paroxysmal activity generated at distant sites within an epileptogenic network contributes to ictal onset patterns observed with the diagnostic macroelectrodes (Bartolomei et al 2001;Wendling et al 2003).…”

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Initiation, Propagation, and Termination of Partial (Focal) Seizures

Curtis

Avoli

2015

Cold Spring Harb Perspect Med

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The neurophysiological patterns that correlate with partial (focal) seizures are well defined in humans by standard electroencephalogram (EEG) and presurgical depth electrode recordings. Seizure patterns with similar features are reproduced in animal models of partial seizures and epilepsy. However, the network determinants that support interictal spikes, as well as the initiation, progression, and termination of seizures, are still elusive. Recent findings show that inhibitory networks are prominently involved at the onset of these seizures, and that extracellular changes in potassium contribute to initiate and sustain seizure progression. The end of a partial seizure correlates with an increase in network synchronization, which possibly involves both excitatory and inhibitory mechanisms.

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Microseizures and the spatiotemporal scales of human partial epilepsy

Cited by 283 publications

References 28 publications

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

Seizure prediction in patients with mesial temporal lobe epilepsy using EEG measures of state similarity

Initiation, Propagation, and Termination of Partial (Focal) Seizures

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