Epilepsy as a derailment of sleep plastic functions may cause chronic cognitive impairment - A theoretical review

Halász, Péter; Ujma, Péter P.; Fabó, Dániel; Bódizs, Róbert; Szücs, Anna

doi:10.1016/j.smrv.2019.01.003

Cited by 18 publications

(19 citation statements)

References 87 publications

(87 reference statements)

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“…When large functional circuits are involved in the pathological process, their function shows abnormalities, and it is demonstrated by the alteration of sleep structure (Palop and Mucke, 2010). Increasing number of epileptic discharges leads to reduction in slow-wave sleep, overproduction of dysfunctional, dummy sleep spindles, and finally loss of sleep function in the memory encoding and consolidation process (Malow, 2007;Halász et al, 2019). Since epileptic discharges are crucial in the pathological process, modification might have a novel therapeutic potential in cognitive disorders (Bakker et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

“…An epileptic spike is shorter but similar to sharp wave, and it associates to faster ripple oscillations than sharp wave ( Bragin et al, 2002 ). Numerous studies hypothesized that epileptic discharges linked to fast ripples could interfere with normal memory process ( Halász et al, 2019 ; Figure 3 ). Furthermore, they can also act as dysfunctional (“dummy”) variants of sharp-wave deteriorating memory consolidation ( Gelinas et al, 2016 ).…”

Section: Mechanism Of Cognitive Impairmentmentioning

confidence: 99%

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Inhibiting Epileptiform Activity in Cognitive Disorders: Possibilities for a Novel Therapeutic Approach

et al. 2020

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Cognitive impairment is a common and seriously debilitating symptom of various mental and neurological disorders including autism, attention deficit hyperactivity disorder, multiple sclerosis, epilepsy, and neurodegenerative diseases, like Alzheimer's disease. In these conditions, high prevalence of epileptiform activity emerges as a common pathophysiological hallmark. Growing body of evidence suggests that this discrete but abnormal activity might have a long-term negative impact on cognitive performance due to neuronal circuitries' remodeling, altered sleep structure, pathological hippocampocortical coupling, and even progressive neuronal loss. In animal models, epileptiform activity was shown to enhance the formation of pathological amyloid and tau proteins that in turn trigger network hyperexcitability. Abolishing epileptiform discharges might slow down the cognitive deterioration. These findings might provide basis for therapeutic use of antiepileptic drugs in neurodegenerative cognitive disorders. The aim of our review is to describe the data on the prevalence of epileptiform activity in various cognitive disorders, to summarize the current knowledge of the mechanisms of epileptic activity in relation to cognitive impairment, and to explore the utility of antiepileptic drugs in the therapy of cognitive disorders. We also propose future directions for drug development and novel therapeutic interventions targeting epileptiform discharges in these disorders.

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Section: Discussionmentioning

confidence: 99%

Section: Mechanism Of Cognitive Impairmentmentioning

confidence: 99%

Inhibiting Epileptiform Activity in Cognitive Disorders: Possibilities for a Novel Therapeutic Approach

et al. 2020

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“…44 This impairment may be secondary to the disruption or hijacking by EA of fine-tuned coupled oscillations involved in sleep-related cognitive processes. [45][46][47] Nocturnal seizures are usually considered as less disabling During pre-arousal time window (ATW), spectral ratio and spike index of mesial channels are highly correlated (r = 0.95, p < 0.0001) with a time shift of −1.2 (delay in ratio fluctuations), whereas for neocortical channels no time shift is observed (r = 0.97, p < 0.0001). During ATW, the spectral ratio variation remains significantly correlated and delayed as compared to the spike index of mesial channels (time shift = −1.6 seconds, r = 0.97, p < 0.0001), whereas a positive time shift is observed for neocortical channels (time shift = + 0.4 seconds, r = 0.99, p < 0.0001).…”

Section: Arousing Effect Of Interictal Activitymentioning

confidence: 99%

Sleep Disruption in Epilepsy: Ictal and Interictal Epileptic Activity Matter

Peter‐Derex

Klimeš

Latreille

et al. 2020

Annals of Neurology

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Objective: Disturbed sleep is common in epilepsy. The direct influence of nocturnal epileptic activity on sleep fragmentation remains poorly understood. Stereo-electroencephalography paired with polysomnography is the ideal tool to study this relationship. We investigated whether sleep-related epileptic activity is associated with sleep disruption. Methods: We visually marked sleep stages, arousals, seizures, and epileptic bursts in 36 patients with focal drugresistant epilepsy who underwent combined stereo-electroencephalography/polysomnography during presurgical evaluation. Epileptic spikes were detected automatically. Spike and burst indices (n/sec/channel) were computed across four 3-second time windows (baseline sleep, pre-arousal, arousal, and post-arousal). Sleep stage and anatomic localization were tested as modulating factors. We assessed the intra-arousal dynamics of spikes and their relationship with the slow wave component of non-rapid eye-movement sleep (NR) arousals. Results: The vast majority of sleep-related seizures (82.4%; 76.5% asymptomatic) were followed by awakenings or arousals. The epileptic burst index increased significantly before arousals as compared to baseline and postarousal, irrespective of sleep stage or brain area. A similar pre-arousal increase was observed for the spike index in NR stage 2 and rapid eye-movement sleep. In addition, the spike index increased during the arousal itself in neocortical channels, and was strongly correlated with the slow wave component of NR arousals (r = 0.99, p < 0.0001). Interpretation: Sleep fragmentation in focal drug-resistant epilepsy is associated with ictal and interictal epileptic activity. The increase in interictal epileptic activity before arousals suggests its participation in sleep disruption. An additional increase in the spike rate during arousals may result from a sleep-wake boundary instability, suggesting a bidirectional relationship.

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“…suggesting that acute transient memory losses, rather than genuine disturbances of consciousness may underlie patients' ictal loss of contact in partial seizures. Hippocampal sclerosis appeared to fully account for the side-specific memory disturbance in MTLE, however, the transformation of sharp-wave ripples (SPW-Rs) to interictal epileptiform discharges (IEDs) obstructing memory consolidation, has made an additional factor ( 31 ).…”

Section: The Epileptic Transformation Of the Hippocampo-frontal Declamentioning

confidence: 99%

Sleep and Epilepsy Link by Plasticity

Halász

Szücs

2020

Front. Neurol.

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We aimed to explore the link between NREM sleep and epilepsy. Based on human and experimental data we propose that a sleep-related epileptic transformation of normal neurological networks underlies epileptogenesis. Major childhood epilepsies as medial temporal lobe epilepsy (MTLE), absence epilepsy (AE) and human perisylvian network (PN) epilepsies - made us good models to study. These conditions come from an epileptic transformation of the affected functional systems. This approach allows a system-based taxonomy instead of the outworn generalized-focal classification. MTLE links to the memory-system, where epileptic transformation results in a switch of normal sharp wave-ripples to epileptic spikes and pathological high frequency oscillations, compromising sleep-related memory consolidation. Absence epilepsy (AE) and juvenile myoclonic epilepsy (JME) belong to the corticothalamic system. The burst-firing mode of NREM sleep normally producing sleep-spindles turns to an epileptic working mode ejecting bilateral synchronous spike-waves. There seems to be a progressive transition from AE to JME. Shared absences and similar bilateral synchronous discharges show the belonging of the two conditions, while the continuous age windows - AE affecting schoolchildren, JME the adolescents - and the increased excitability in JME compared to AE supports the notion of progression. In perisylvian network epilepsies - idiopathic focal childhood epilepsies and electrical status epilepticus in sleep including Landau-Kleffner syndrome - centrotemporal spikes turn epileptic, with the potential to cause cognitive impairment. Postinjury epilepsies modeled by the isolated cortex model highlight the shared way of epileptogenesis suggesting the derailment of NREM sleep-related homeostatic plasticity as a common step. NREM sleep provides templates for plasticity derailing to epileptic variants under proper conditions. This sleep-origin explains epileptiform discharges' link and similarity with NREM sleep slow oscillations, spindles and ripples. Normal synaptic plasticity erroneously overgrowing homeostatic processes may derail toward an epileptic working-mode manifesting the involved system's features. The impact of NREM sleep is unclear in epileptogenesis occurring in adolescence and adulthood, when plasticity is lower. The epileptic process interferes with homeostatic synaptic plasticity and may cause cognitive impairment. Its type and degree depends on the affected network's function. We hypothesize a vicious circle between sleep end epilepsy. The epileptic derailment of normal plasticity interferes with sleep cognitive functions. Sleep and epilepsy interconnect by the pathology of plasticity.

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Epilepsy as a derailment of sleep plastic functions may cause chronic cognitive impairment - A theoretical review

Cited by 18 publications

References 87 publications

Inhibiting Epileptiform Activity in Cognitive Disorders: Possibilities for a Novel Therapeutic Approach

Inhibiting Epileptiform Activity in Cognitive Disorders: Possibilities for a Novel Therapeutic Approach

Sleep Disruption in Epilepsy: Ictal and Interictal Epileptic Activity Matter

Sleep and Epilepsy Link by Plasticity

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