EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans

Frauscher, Birgit; Ellenrieder, Nicolás von; Dubeau, François; Gotman, Jean

doi:10.1111/epi.13389

Cited by 99 publications

(84 citation statements)

References 39 publications

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“…In a previous work, we showed that physiological HFOs are closely linked to phasic REM sleep (Frauscher et al, 2016), which is suggested to play an important role in learning and memory (Buzsáki et al, 1992, Datta, 2000, Datta et al, 2004, Diekelmann et al, 2009). …”

Section: Discussionmentioning

confidence: 99%

Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties

Ellenrieder

Dubeau

Gotman

et al. 2017

NeuroImage: Clinical

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ObjectiveThe stage of sleep is a known modulator of high-frequency oscillations (HFOs). For instance, high amplitude slow waves during NREM sleep and the subtypes of REM sleep were shown to contribute to a better separation between physiological and pathological HFOs. This study investigated rates and spatial spread of the different HFO types (physiological and pathological ripples in the 80–250 Hz frequency band, and fast ripples above 250 Hz) depending on time spent in sleep across the different sleep cycles.MethodsFifteen patients with focal pharmaco-resistant epilepsy underwent one night of video-polysomnography during chronic intracranial EEG recording for presurgical epilepsy evaluation. The HFO rate and spread across the different sleep cycles were determined with an automatic HFO detector. We built models to explain the observed rate and spread based on time in sleep and other variables i.e. sleep stage, delta band and sigma band activity, and slow wave amplitude. Statistical significance of the different variables was determined by a model comparison using the Akaike information criterion.ResultsThe rate of HFOs depends significantly on the accumulated time of sleep. As the night advanced, the rate of pathological ripples and fast ripples decreased during NREM sleep (up to 15% per hour spent in the respective sleep stages), while the rate of physiological ripples increased during REM sleep (8% per hour spent in REM sleep). Interestingly, the stage of sleep but not the sleep cycle determined the extent of spread of HFOs, showing a larger field during NREM sleep and a more restricted field during REM sleep.ConclusionThe different dependence with sleep time for physiological and pathological ripples is in keeping with their distinct underlying generating mechanisms. From a practical point of view, the first sleep cycle seems to be best suitable for studying HFOs in epilepsy, given that the contrast between physiological and pathological ripple rates is largest during this time.

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Section: Discussionmentioning

confidence: 99%

Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties

Ellenrieder

Dubeau

Gotman

et al. 2017

NeuroImage: Clinical

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100

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“…Cortical slow waves during non‐REM sleep modulate the occurrence of interictal spikes and ripples in epileptic patients: higher rates of interictal spikes and higher ripple density are observed during high‐amplitude, widespread slow waves recorded from scalp electrodes than during control segments that are obtained during the same sleep stage (Frauscher et al ., ). A follow‐up study has revealed that ripples in the epileptogenic zone and in non‐epileptogenic zones behave differently during phasic and tonic REM sleep: in non‐epileptogenic zones, ripple rates increase during phasic REM sleep, but they increase in the epileptogenic zone during tonic REM sleep (Frauscher et al ., ). Therefore, these data suggest that ripples are reliable biomarkers of seizure onset zones only when their relationship with other electrophysiological events, such as cortical slow waves or interictal spikes, is taken into account.…”

Section: Correlation Between Interictal Spikes and Hfosmentioning

confidence: 97%

Interictal oscillations and focal epileptic disorders

Lévesque

Salami

Shiri

et al. 2017

Eur J of Neuroscience

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Neuronal network oscillations represent a main feature of the brain activity recorded in the EEG under normal and pathological conditions such as epilepsy. Specific oscillations occur between seizures in patients and in animal models of focal epilepsy, and thus, they are termed interictal. According to their shape and intrinsic signal frequency, interictal oscillations are classified as spikes and high-frequency oscillations (HFOs). Interictal spikes are recorded in the 'wideband' EEG signal and consist of large-amplitude events that usually last less than 1 s; HFOs, in contrast, are extracted by amplifying the appropriately filtered EEG signal and are usually categorized as ripples (80-200 Hz) and fast ripples (250-500 Hz). Interictal spikes and HFOs are used in clinical practice to localize the seizure onset zone in focal epileptic disorders, which is fundamental for performing successful surgical interventions in epileptic patients not responding to anti-epileptic drug therapy. Both types of interictal oscillations have been widely studied in animal models of focal epilepsy to identify the mechanisms underlying their generation as well as to establish their role in ictogenesis and epileptogenesis. In this review, we will address the cellular mechanisms underlying the generation of interictal spikes and HFOs in animal models of epileptiform synchronization and of focal epilepsy. Moreover, we will highlight in vitro and in vivo evidence indicating that these interictal oscillations mirror specific, dynamic changes in neuronal network excitability causing seizure generation (i.e. ictogenesis) and leading to a chronic epileptic condition (i.e. epileptogenesis).

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“…In contrast to ripples in the SOZ or exclusively irritative zone, physiologic ripples were more abundant during phasic REM sleep. 83 It may therefore be more important to know the EEG context of occurrence of an HFO than its morphology to determine whether it is normal or pathological.…”

Section: Differentiation Between Physiological and Pathological Hfosmentioning

confidence: 99%

High‐frequency oscillations: The state of clinical research

et al. 2017

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Summary Modern electroencephalographic (EEG) technology contributed to the appreciation that the EEG signal outside the classical Berger frequency band contains important information. In epilepsy, research of the past decade focused particularly on interictal high-frequency oscillations (HFOs) > 80 Hz. The first large application of HFOs was in the context of epilepsy surgery. This is now followed by other applications such as assessment of epilepsy severity and monitoring of antiepileptic therapy. This article reviews the evidence on the clinical use of HFOs in epilepsy with an emphasis on the latest developments. It highlights the growing literature on the association between HFOs and post-surgical seizure outcome. A recent meta-analysis confirmed a higher resection ratio for HFOs in seizure-free versus non–seizure-free patients. Residual HFOs in the postoperative electrocorticogram were shown to predict epilepsy surgery outcome better than preoperative HFO rates. The review further discusses the different attempts to separate physiological from epileptic HFOs, as this might increase the specificity of HFOs. As an example, analysis of sleep microstructure demonstrated a different coupling between HFOs inside and outside the epileptogenic zone. Moreover, there is increasing evidence that HFOs are useful to measure disease activity and assess treatment response using noninvasive EEG and magnetoencephalography. This approach is particularly promising in children, because they show high scalp HFO rates. HFO rates in West syndrome decrease after adrenocorticotropic hormone treatment. Presence of HFOs at the time of rolandic spikes correlates with seizure frequency. The time-consuming visual assessment of HFOs, which prevented their clinical application in the past, is now overcome by validated computer-assisted algorithms. HFO research has considerably advanced over the past decade, and use of noninvasive methods will make HFOs accessible to large numbers of patients. Prospective multicenter trials are awaited to gather information over long recording periods in large patient samples.

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EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans

Cited by 99 publications

References 39 publications

Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties

Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties

Interictal oscillations and focal epileptic disorders

High‐frequency oscillations: The state of clinical research

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