Does epileptic activity impair sleep-related memory consolidation in epilepsy? A critical and systematic review

Latreille, Véronique; Schiller, Katharina; Peter‐Derex, Laure; Frauscher, Birgit

doi:10.5664/jcsm.10166

Cited by 7 publications

(4 citation statements)

References 59 publications

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“…Recent studies provide compelling evidence that the overnight decrease in slope is critically dampened in childhood epilepsies with spike-wave activation during sleep 22 – 25 . Interestingly, these same patient group shows significant deficits in sleep-dependent memory consolidation 26 . It is tempting to assume that impaired consolidation of newly learned information might lead with time to the patient’s behavioral and cognitive deficits.…”

Section: Introductionmentioning

confidence: 84%

Automated analysis of a large-scale paediatric dataset illustrates the interdependent relationship between epilepsy and sleep

Skorucak

Bölsterli

Storz

et al. 2023

Sci Rep

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Slow waves are an electrophysiological characteristic of non-rapid eye movement sleep and a marker of the restorative function of sleep. In certain pathological conditions, such as different types of epilepsy, slow-wave sleep is affected by epileptiform discharges forming so-called “spike-waves”. Previous evidence shows that the overnight change in slope of slow waves during sleep is impaired under these conditions. However, these past studies were performed in a small number of patients, considering only short segments of the recording night. Here, we screened a clinical data set of 39′179 pediatric EEG recordings acquired in the past 25 years (1994–2019) at the University Children’s Hospital Zurich and identified 413 recordings of interest. We applied an automated approach based on machine learning to investigate the relationship between sleep and epileptic spikes in this large-scale data set. Our findings show that the overnight change in the slope of slow waves was correlated with the spike-wave index, indicating that the impairment of the net reduction in synaptic strength during sleep is spike dependent.

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Section: Introductionmentioning

confidence: 84%

Automated analysis of a large-scale paediatric dataset illustrates the interdependent relationship between epilepsy and sleep

Skorucak

Bölsterli

Storz

et al. 2023

Sci Rep

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“…Among the patients with epilepsy, the effects of sleep on memory retention seem to be comparable to those found in healthy controls [23]. However, nocturnal seizures [24] and sleep-related interictal epileptiform activity [25][26][27][28] impact sleep and, consequently, cognitive function [29].…”

Section: Introductionmentioning

confidence: 84%

Movement Termination of Slow-Wave Sleep—A Potential Biomarker?

Höller,

Eyjólfsdóttir,

Rusiňák

et al. 2024

Brain Sciences

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The duration of slow-wave sleep (SWS) is related to the reported sleep quality and to the important variables of mental and physical health. The internal cues to end an episode of SWS are poorly understood. One such internal cue is the initiation of a body movement, which is detectable as electromyographic (EMG) activity in sleep-electroencephalography (EEG). In the present study, we characterized the termination of SWS episodes by movement to explore its potential as a biomarker. To this end, we characterized the relation between the occurrence of SWS termination by movement and individual characteristics (age, sex), SWS duration and spectral content, chronotype, depression, medication, overnight memory performance, and, as a potential neurological application, epilepsy. We analyzed 94 full-night EEG-EMG recordings (75/94 had confirmed epilepsy) in the video-EEG monitoring unit of the EpiCARE Centre Salzburg, Austria. Segments of SWS were counted and rated for their termination by movement or not through the visual inspection of continuous EEG and EMG recordings. Multiple linear regression was used to predict the number of SWS episodes that ended with movement by depression, chronotype, type of epilepsy (focal, generalized, no epilepsy, unclear), medication, gender, total duration of SWS, occurrence of seizures during the night, occurrence of tonic-clonic seizures during the night, and SWS frequency spectra. Furthermore, we assessed whether SWS movement termination was related to overnight memory retention. According to multiple linear regression, patients with overall longer SWS experienced more SWS episodes that ended with movement (t = 5.64; p = 0.001). No other variable was related to the proportion of SWS that ended with movement, including no epilepsy-related variable. A small sample (n = 4) of patients taking Sertraline experienced no SWS that ended with movement, which was significant compared to all other patients (t = 8.00; p < 0.001) and to n = 35 patients who did not take any medication (t = 4.22; p < 0.001). While this result was based on a small subsample and must be interpreted with caution, it warrants replication in a larger sample with and without seizures to further elucidate the role of the movement termination of SWS and its potential to serve as a biomarker for sleep continuity and for medication effects on sleep.

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“…People with epilepsy are vulnerable to effects of impaired sleep-dependent memory consolidation ( Latreille et al, 2022 ) because of the bi-directional relationship between epilepsy and sleep ( Malow, 2007 ) and, more specifically, because of the negative effects of epilepsy on sleep architecture including fragmentation of slow wave sleep ( López-Gomáriz et al, 2004 ). Among these effects, sleep-dependent interictal epileptiform events particularly during non-REM sleep ( Urbain et al, 2011 ; Bjørnæs et al, 2013 ; Galer et al, 2015 ; Halász et al, 2019 ) and sleep-related seizures ( Malow, 2007 ) partly explain hampered sleep-related memory consolidation in people with epilepsy.…”

Section: Introductionmentioning

confidence: 99%

“…As a general limitation, the sizes of the patient samples in the studies examining overnight memory retention are all very small, limiting possibilities for statistical assessment of multiple moderating factors of overnight retention and therefore restricting overall conclusions ( Latreille et al, 2022 ). It is still unclear whether SWS duration and spectral characteristics as well as other factors such as medication and seizures during the retention interval impact all memory modalities equally.…”

Section: Introductionmentioning

confidence: 99%

The effects of slow wave sleep characteristics on semantic, episodic, and procedural memory in people with epilepsy

Höller,

Eyjólfsdóttir,

Van Schalkwijk

et al. 2024

Front. Pharmacol.

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Slow wave sleep (SWS) is highly relevant for verbal and non-verbal/spatial memory in healthy individuals, but also in people with epilepsy. However, contradictory findings exist regarding the effect of seizures on overnight memory retention, particularly relating to procedural and non-verbal memory, and thorough examination of episodic memory retention with ecologically valid tests is missing. This research explores the interaction of SWS duration with epilepsy-relevant factors, as well as the relation of spectral characteristics of SWS on overnight retention of procedural, verbal, and episodic memory. In an epilepsy monitoring unit, epilepsy patients (N = 40) underwent learning, immediate and 12 h delayed testing of memory retention for a fingertapping task (procedural memory), a word-pair task (verbal memory), and an innovative virtual reality task (episodic memory). We used multiple linear regression to examine the impact of SWS duration, spectral characteristics of SWS, seizure occurrence, medication, depression, seizure type, gender, and epilepsy duration on overnight memory retention. Results indicated that none of the candidate variables significantly predicted overnight changes for procedural memory performance. For verbal memory, the occurrence of tonic-clonic seizures negatively impacted memory retention and higher psychoactive medication load showed a tendency for lower verbal memory retention. Episodic memory was significantly impacted by epilepsy duration, displaying a potential nonlinear impact with a longer duration than 10 years negatively affecting memory performance. Higher drug load of anti-seizure medication was by tendency related to better overnight retention of episodic memory. Contrary to expectations longer SWS duration showed a trend towards decreased episodic memory performance. Analyses on associations between memory types and EEG band power during SWS revealed lower alpha-band power in the frontal right region as significant predictor for better episodic memory retention. In conclusion, this research reveals that memory modalities are not equally affected by important epilepsy factors such as duration of epilepsy and medication, as well as SWS spectral characteristics.

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Does epileptic activity impair sleep-related memory consolidation in epilepsy? A critical and systematic review

Cited by 7 publications

References 59 publications

Automated analysis of a large-scale paediatric dataset illustrates the interdependent relationship between epilepsy and sleep

Automated analysis of a large-scale paediatric dataset illustrates the interdependent relationship between epilepsy and sleep

Movement Termination of Slow-Wave Sleep—A Potential Biomarker?

The effects of slow wave sleep characteristics on semantic, episodic, and procedural memory in people with epilepsy

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