High frequency oscillations and seizure frequency in patients with focal epilepsy

Zijlmans, Maeike; Jacobs, Julia; Zelmann, Rina; Dubeau, François; Gotman, Jean

doi:10.1016/j.eplepsyres.2009.03.026

Cited by 48 publications

(36 citation statements)

References 17 publications

(16 reference statements)

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“…These latter findings are consistent with previous studies that used recordings from NREM episodes to characterize spatial patterns of interictal HFOs in relation to seizure-onset areas [28, 30••, 31, 46, 47] and rates of interictal HFOs with respect to seizure frequency [48]. …”

Section: High-frequency Oscillations In Patients With Epilepsysupporting

confidence: 92%

High-frequency oscillations in epileptic brain

Bragin¹,

Engel

Staba³

2010

Current Opinion in Neurology

177

153

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Purpose of review It has been 10 years since pathological high-frequency oscillations (pHFOs) were described in the brain of epileptic animals and patients. This review summarizes progress in research on mechanisms of their generation and potential clinical applications over that period. Recent findings Initially, pHFOs were recorded with microelectrodes in the hippocampus of rodents and patients with mesial temporal lobe epilepsy (MTLE), but recently pHFOs have also been recorded with clinical depth and grid electrodes in multiple brain areas including the hippocampus and neocortex of patients with different types of epilepsy. One hypothesis is that pHFOs reflect fields of hypersynchronized action potentials (bursts of population spikes) within small discrete neuronal clusters responsible for seizure generation. Studies suggest that pHFOs can be used as a reliable biomarker for epileptogenesis, epileptogenicity, and the delineation of the epileptogenic region. Summary Recording of pHFOs with clinical electrodes provides a means for further investigation of their functional role in the epileptic brain and as a potential biomarker of epileptogenesis and epileptogenicity and for presurgical mapping.

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Section: High-frequency Oscillations In Patients With Epilepsysupporting

confidence: 92%

High-frequency oscillations in epileptic brain

Bragin¹,

Engel

Staba³

2010

Current Opinion in Neurology

177

153

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“…Evidence obtained from in vitro 47 and in vivo 6,7 animal models as well as from epileptic patients 48 indicates that HFO rate of occurrence increases shortly before the appearance of ictal activity and remains high throughout. Ripples occur when inhibitory interneurons entrain pyramidal cells and other interneurons into a rhythmic pattern of firing.…”

Section: High-frequency Oscillations Associated With Lvf and Hyp Onsementioning

confidence: 99%

Activation of specific neuronal networks leads to different seizure onset types

Shiri

Manseau

Lévesque

et al. 2016

Annals of Neurology

100

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Objective-Ictal events occurring in temporal lobe epilepsy patients and in experimental models mimicking this neurological disorder can be classified, based on their onset pattern, into lowvoltage, fast versus hypersynchronous onset seizures. It has been suggested that the low-voltage, fast onset pattern is mainly contributed by interneuronal (γ-aminobutyric acidergic) signaling, whereas the hypersynchronous onset involves the activation of principal (glutamatergic) cells.Methods-Here, we tested this hypothesis using the optogenetic control of parvalbumin-positive or somatostatin-positive interneurons and of calmodulin-dependent, protein kinase-positive, principal cells in the mouse entorhinal cortex in the in vitro 4-aminopyridine model of epileptiform synchronization.Results-We found that during 4-aminopyridine application, both spontaneous seizure-like events and those induced by optogenetic activation of interneurons displayed low-voltage, fast onset patterns that were associated with a higher occurrence of ripples than of fast ripples. In contrast, seizures induced by the optogenetic activation of principal cells had a hypersynchronous onset pattern with fast ripple rates that were higher than those of ripples.Interpretation-Our results firmly establish that under a similar experimental condition (ie, bath application of 4-aminopyridine), the initiation of low-voltage, fast and of hypersynchronous onset seizures in the entorhinal cortex depends on the preponderant involvement of interneuronal and principal cell networks, respectively.Seizures in patients presenting with temporal lobe epilepsy (TLE) are mainly characterized by 2 distinct electrographic onset patterns, defined as low-voltage, fast (LVF) and hypersynchronous (HYP). 1,2 LVF seizures are characterized at onset by the occurrence of a sentinel spike followed by low-amplitude, high-frequency activity, whereas the initiation of Recently, the analysis of high-frequency oscillations (HFOs; ripples: 80-200Hz, fast ripples: 250-500Hz) during spontaneous HYP and LVF seizures in the pilocarpine and kainic acid model of TLE has suggested that these 2 seizure onset patterns may rely on distinct mechanisms of initiation. LVF seizures were found to be mainly associated with HFOs in the ripple frequency range, thus suggesting the predominant involvement of interneuronal (inhibitory) networks; in contrast, HYP seizures were mostly accompanied by fast ripple occurrence, thus highlighting the potential role of principal (glutamatergic) networks. 6,7 Evidence obtained to date suggests that pathologic HFOs in the ripple band should represent population inhibitory postsynaptic potentials generated by principal neurons entrained by synchronously active interneuron networks, whereas those in the fast ripple band reflect the synchronous firing of abnormally active principal cells, and thus are not dependent on inhibitory processes. [8][9][10] It has been demonstrated that 4-aminopyridine (4AP) application induces LVF onset discharges in several limbic and para...

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“…HFOs are mainly related to interictal spikes and are state-dependent since they occur more frequently during slow-wave sleep (Bagshaw et al, 2009;Bragin et al, 2000;Staba et al, 2004). Higher HFO rates are significantly correlated with higher seizure frequency in epileptic patients (Ziljmans et al, 2009), and appear to be more specific markers than interictal spikes in identifying the seizure onset zone, independently of the underlying pathology (Crépon et al, 2010;Jacobs et al, 2008;. Moreover, the spatial distribution of HFOs in the epileptogenic zone depends on the type of epileptic discharge, as widespread interictal spikes propagating across multiple cortical regions are often related to HFOs that can be recorded on multiple channels (Schevon et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

High-frequency (80–500Hz) oscillations and epileptogenesis in temporal lobe epilepsy

Lévesque

Bortel

Gotman

et al. 2011

Neurobiology of Disease

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High-frequency oscillations (HFOs), termed ripples and fast ripples , are recorded in the EEG of epileptic patients and in animal epilepsy models; HFOs are thought to reect pathological activity and seizure onset zones. Here, we analyzed the temporal and spatial evolution of interictal spikes with and without HFOs in the rat pilocarpine model of temporal lobe epilepsy. Depth electrode recordings from dentate gyrus (DG), CA3 region, subiculum and entorhinal cortex (EC), were obtained from rats between the 4th and 15th day after a status epilepticus (SE) induced by i.p. injection of pilocarpine. The first seizure occurred 6.1±2.5 days after SE (n=7 rats). Five of 7 animals exhibited interictal spikes that co-occurred with fast ripples accounting for 4.9±4.6% of all analyzed interictal spikes (n=12,886) while all rats showed interictal spikes co-occurring with ripples, accounting for 14.3±3.4% of all events. Increased rates of interictal spikes without HFOs in the EC predicted upcoming seizures on the following day, while rates of interictal spikes with fast ripples in CA3 reflected periods of high seizure occurrence. Finally, interictal spikes co-occurring with ripples did not show any specific relation to seizure occurrence. Our findings identify different temporal and spatial developmental patterns for the rates of interictal spikes with or without HFOs in relation with seizure occurrence. These distinct categories of interictal spikes point at dynamic processes that should bring neuronal networks close to seizure generation.

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High frequency oscillations and seizure frequency in patients with focal epilepsy

Cited by 48 publications

References 17 publications

High-frequency oscillations in epileptic brain

High-frequency oscillations in epileptic brain

Activation of specific neuronal networks leads to different seizure onset types

High-frequency (80–500Hz) oscillations and epileptogenesis in temporal lobe epilepsy

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