Dataset Information

Interictal Hippocampal Spiking Influences the Occurrence of Hippocampal Sleep Spindles.

ABSTRACT:

Objectives

The significance of hippocampal sleep spindles and their relation to epileptic activity is still a matter of controversy. Hippocampal spindles have been considered a physiological phenomenon, an evoked response to afferent epileptic discharges, or even the expression of an epileptic manifestation. To address this question, we investigated the presence and rate of hippocampal spindles in focal pharmacoresistant epilepsy patients undergoing scalp-intracerebral electroencephalography (EEG).

Design

Sleep recording with scalp-intracerebral EEG.

Setting

Tertiary referral epilepsy center.

Patients

Twenty-five epilepsy patients (extratemporal: n = 6, temporal: n = 15, and multifocal including the temporal lobe: n = 4).

Interventions

N/A.

Measurements and results

We analyzed associations between hippocampal spindles and hippocampal electrophysiological findings (interictal spiking, seizure onset zone) and magnetic resonance imaging volumetry. Sixteen of 25 patients (64%) had hippocampal spindles (extratemporal epilepsy: 6/6; temporal epilepsy: 10/15; and multifocal epilepsy: 0/4; P = 0.005). Median spindle rate was 0.6 (range, 0.1-8.6)/min in nonrapid eye movement sleep. Highest spindle rates were found in hippocampi of patients with extratemporal epilepsy (P < 0.001). A negative association was found between hippocampal spiking activity and spindle rate (P = 0.003). We found no association between the presence (n = 21) or absence (n = 17) of hippocampal seizure onset zone and hippocampal spindle rate (P = 0.114), and between a normal (n = 30) or atrophic (n = 8) hippocampus and hippocampal spindle rate (P = 0.195).

Conclusions

Hippocampal spindles represent a physiological phenomenon, with an expression that is diminished in epilepsy affecting the temporal lobe. Hippocampal spiking lowered the rate of hippocampal spindles, suggesting that epileptic discharges may at least in part be a transformation of these physiological events, similar to the hypothesis considering generalized spike-and-waves a transformation of frontal spindles.

SUBMITTER: Frauscher B

PROVIDER: S-EPMC4667386 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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Publications

Interictal Hippocampal Spiking Influences the Occurrence of Hippocampal Sleep Spindles.

Frauscher Birgit B Bernasconi Neda N Caldairou Benoit B von Ellenrieder Nicolás N Bernasconi Andrea A Gotman Jean J Dubeau François F

Sleep 20151201 12

<h4>Objectives</h4>The significance of hippocampal sleep spindles and their relation to epileptic activity is still a matter of controversy. Hippocampal spindles have been considered a physiological phenomenon, an evoked response to afferent epileptic discharges, or even the expression of an epileptic manifestation. To address this question, we investigated the presence and rate of hippocampal spindles in focal pharmacoresistant epilepsy patients undergoing scalp-intracerebral electroencephalogr ...[more]

PMID: 26194569

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Project description:PurposeInterictal epileptic discharges (IEDs) are known to affect cognitive function in patients with epilepsy, but the mechanism has not been elucidated. Sleep spindles appearing in synchronization with IEDs were recently demonstrated to impair memory consolidation in rat, but this has not been investigated in humans. On the other hand, the increase of sleep spindles at night after learning is positively correlated with amplified learning effects during sleep for motor sequence learning. In this study, we examined the effects of IEDs and IED-coupled spindles on motor sequence learning in patients with epilepsy, and clarified their pathological significance.Materials and methodsPatients undergoing long-term video-electroencephalography (LT-VEEG) at our hospital from June 2019 to November 2021 and age-matched healthy subjects were recruited. Motor sequence learning consisting of a finger-tapping task was performed before bedtime and the next morning, and the improvement rate of performance was defined as the sleep-dependent learning effect. We searched for factors associated with the changes in learning effect observed between the periods of when antiseizure medications (ASMs) were withdrawn for LT-VEEG and when they were returned to usual doses after LT-VEEG.ResultsExcluding six patients who had epileptic seizures at night after learning, nine patients and 11 healthy subjects were included in the study. In the patient group, there was no significant learning effect when ASMs were withdrawn. The changes in learning effect of the patient group during ASM withdrawal were not correlated with changes in sleep duration or IED density; however, they were significantly negatively correlated with changes in IED-coupled spindle density.ConclusionWe found that the increase of IED-coupled spindles correlated with the decrease of sleep-dependent learning effects of procedural memory. Pathological IED-coupled sleep spindles could hinder memory consolidation, that is dependent on physiological sleep spindles, resulting in cognitive dysfunction in patients with epilepsy.

Dataset Information

Interictal Hippocampal Spiking Influences the Occurrence of Hippocampal Sleep Spindles.

Objectives

Design

Setting

Patients

Interventions

Measurements and results

Conclusions

Publications

Interictal Hippocampal Spiking Influences the Occurrence of Hippocampal Sleep Spindles.

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