Remission of encephalopathy with status epilepticus (ESES) during sleep renormalizes regulation of slow wave sleep

Bölsterli, Bigna K.; Gardella, Elena; Pavlidis, Elena; Wehrle, Flavia M.; Tassinari, C. A.; Huber, Reto; Rubboli, Guido

doi:10.1111/epi.13910

Cited by 52 publications

(33 citation statements)

References 40 publications

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“…It has long been postulated that the unfavorable cognitive outcome of EAS disorders is at least partly caused by epileptiform activity during sleep; the analysis of SWS might consequently serve as a prognosis factor for cognitive outcome in EAS patients . As early as the 3rd postnatal week, Grin2a KO mice displayed altered hippocampal LTP, which worsened with time and persisted in adulthood .…”

Section: Discussionmentioning

confidence: 99%

Impaired vocal communication, sleep‐related discharges, and transient alteration of slow‐wave sleep in developing mice lacking the GluN2A subunit of N‐methyl‐d‐aspartate receptors

et al. 2019

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Objective Glutamate‐gated N‐methyl‐d‐aspartate receptors (NMDARs) are instrumental to brain development and functioning. Defects in the GRIN2A gene, encoding the GluN2A subunit of NMDARs, cause slow‐wave sleep (SWS)‐related disorders of the epilepsy‐aphasia spectrum (EAS). The as‐yet poorly understood developmental sequence of early EAS‐related phenotypes, and the role of GluN2A‐containing NMDARs in the development of SWS and associated electroencephalographic (EEG) activity patterns, were investigated in Grin2a knockout (KO) mice. Methods Early social communication was investigated by ultrasonic vocalization (USV) recordings; the relationship of electrical activity of the cerebral cortex with SWS was studied using deep local field potential or chronic EEG recordings at various postnatal stages. Results Grin2a KO pups displayed altered USV and increased occurrence of high‐voltage spindles. The pattern of slow‐wave activity induced by low‐dose isoflurane was altered in Grin2a KO mice in the 3rd postnatal week and at 1 month of age. These alterations included strong suppression of the delta oscillation power and an increase in the occurrence of the spike‐wave bursts. The proportion of SWS and the sleep quality were transiently reduced in Grin2a KO mice aged 1 month but recovered by the age of 2 months. Grin2a KO mice also displayed spontaneous spike‐wave discharges, which occurred nearly exclusively during SWS, at 1 and 2 months of age. Significance The impaired vocal communication, the spike‐wave discharges occurring almost exclusively in SWS, and the age‐dependent alteration of SWS that were all seen in Grin2a KO mice matched the sleep‐related and age‐dependent manifestations seen in children with EAS, hence validating the Grin2a KO as a reliable model of EAS disorders. Our data also show that GluN2A‐containing NMDARs are involved in slow‐wave activity, and that the period of postnatal brain development (postnatal day 30) when several anomalies peaked might be critical for GluN2A‐dependent, sleep‐related physiological and pathological processes.

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Section: Discussionmentioning

confidence: 99%

Impaired vocal communication, sleep‐related discharges, and transient alteration of slow‐wave sleep in developing mice lacking the GluN2A subunit of N‐methyl‐d‐aspartate receptors

et al. 2019

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“…In one child, hydrocortisone treatment normalized both the sleep EEG and overnight performance (another child whose EEG was only partially improved showed no improvement), suggesting that the impairment of sleep homeostasis may be responsible for the lack of memory consolidation. Finally, Boelsterli et al (2017) reduced overnight slope decline of sleep slow waves has been shown to be related to poorer learning during wakefulness also in adult patients with focal epilepsy (Boly et al, 2017).…”

Section: Impaired Synaptic Homeostasis In Esesmentioning

confidence: 96%

Encephalopathy related to Status Epilepticus during slow Sleep: a link with sleep homeostasis?

Rubboli

Huber

Tononi

et al. 2019

Epileptic Disorders

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Encephalopathy related to Status Epilepticus during slow Sleep (ESES) is a childhood epilepsy syndrome characterized by appearance of cognitive and behavioural disturbances in conjunction with a striking activation of EEG epileptic abnormalities during sleep. The link between the extreme amount of epileptic discharges during sleep and the deterioration of cognitive functions and behavior is poorly understood. We hypothesize that the negative effects of ESES may depend on the impairment of the synaptic homeostasis processes occurring during normal sleep and that are particularly important in the developmental age. Sleep ensures synaptic homeostasis by promoting synaptic weakening/elimination after the increase of synaptic strength that occurs during wakefulness. Changes in synaptic strength are reflected in the EEG by changes of sleep slow wave activity (SWA). Recent studies in ESES have failed to show changes of sleep SWA, particularly at the site of the epileptic focus, suggesting a spike‐related impairment of the homeostatic recovery of sleep. This impaired synaptic homeostasis in the critical period of development may alter cortical wiring and thereby disrupt, often irreversibly, cognitive functions and behavior, leading to the neuropsychological compromise typical of ESES.

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“…Based on these data, it has been hypothesized that prolonged, sleep-related focal epileptic activity interferes with sleep slow wave activity, particularly at the site of the epileptic focus, hence disrupting the cortical plasticity processes occurring during sleep that are necessary for learning and memory consolidation of what has been acquired in wakefulness, ultimately resulting in neuropsychological and behavioural disorders (Tassinari and Rubboli, 2006). In fact, some recent reports support this hypothesis, by providing electrophysiological evidence that physiological parameters related to NREM slow-wave activity are impaired in children with ESES and recover after ESES resolution (Bölsterli et al, 2011(Bölsterli et al, , 2017. These concepts, that provide a fascinating pathophysiological explanation linking the cognitive impairment to the sleep-related exaggerated epileptic activity that characterize ESES, are efficaciously conveyed by the eponym "Penelope syndrome" in which the 'cognitive threads' (neuronal networks) that are weaved during the day are unravelled (by continuous "spiking") during the night (Tassinari et al, 2009 None of the authors have any conflict of interest to declare.…”

Section: Encephalopathy Related To Status Epilepticus During Slow Slementioning

confidence: 99%

Encephalopathy related to Status Epilepticus during slow Sleep: an historical introduction

Rubboli

Tassinari

2019

Epileptic Disorders

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Remission of encephalopathy with status epilepticus (ESES) during sleep renormalizes regulation of slow wave sleep

Cited by 52 publications

References 40 publications

Impaired vocal communication, sleep‐related discharges, and transient alteration of slow‐wave sleep in developing mice lacking the GluN2A subunit of N‐methyl‐d‐aspartate receptors

Impaired vocal communication, sleep‐related discharges, and transient alteration of slow‐wave sleep in developing mice lacking the GluN2A subunit of N‐methyl‐d‐aspartate receptors

Encephalopathy related to Status Epilepticus during slow Sleep: a link with sleep homeostasis?

Encephalopathy related to Status Epilepticus during slow Sleep: an historical introduction

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