Hijacking of hippocampal–cortical oscillatory coupling during sleep in temporal lobe epilepsy

Mendes, Renan Augusto Viana; Zacharias, Leonardo Rakauskas; Ruggiero, Rafael Naime; Leite, João Pereira; Moraes, Márcio Flávio Dutra; Lopes-Aguiar, Cleiton

doi:10.1016/j.yebeh.2019.106608

Cited by 13 publications

(10 citation statements)

References 38 publications

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“…A direct effect of nocturnal discharges is also suspected, as sleep‐related memory consolidation in patients with epilepsy may be impaired in case of sleep‐related EA 44 . This impairment may be secondary to the disruption or hijacking by EA of fine‐tuned coupled oscillations involved in sleep‐related cognitive processes 45–47 . Nocturnal seizures are usually considered as less disabling than diurnal seizures, especially regarding driving or professional activities.…”

Section: Discussionmentioning

confidence: 99%

“…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%

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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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Section: Discussionmentioning

confidence: 99%

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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“…Chronic ketamine treatment also causes long-term alterations on theta-gamma CFC depending on the behavioral state 64 . Theta oscillations are prominent during exploratory activity 65 and theta-gamma CFC has been related to working memory and memory consolidation mechanisms [66][67][68] .…”

Section: Discussionmentioning

confidence: 99%

Long-term potentiation prevents ketamine-induced aberrant neurophysiological dynamics in the hippocampus-prefrontal cortex pathway in vivo

Lopes-Aguiar

Ruggiero

Rossignoli

et al. 2020

Sci Rep

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N-methyl-D-aspartate receptor (NMDAr) antagonists such as ketamine (KET) produce psychotic-like behavior in both humans and animal models. NMDAr hypofunction affects normal oscillatory dynamics and synaptic plasticity in key brain regions related to schizophrenia, particularly in the hippocampus and the prefrontal cortex. It has been shown that prior long-term potentiation (LTP) occluded the increase of synaptic efficacy in the hippocampus-prefrontal cortex pathway induced by MK-801, a noncompetitive NMDAr antagonist. However, it is not clear whether LTP could also modulate aberrant oscillations and short-term plasticity disruptions induced by NMDAr antagonists. Thus, we tested whether LTP could mitigate the electrophysiological changes promoted by KET. We recorded HPC-PFC local field potentials and evoked responses in urethane anesthetized rats, before and after KET administration, preceded or not by LTP induction. Our results show that KET promotes an aberrant delta-high-gamma cross-frequency coupling in the PFC and an enhancement in HPC-PFC evoked responses. LTP induction prior to KET attenuates changes in synaptic efficiency and prevents the increase in cortical gamma amplitude comodulation. These findings are consistent with evidence that increased efficiency of glutamatergic receptors attenuates cognitive impairment in animal models of psychosis. Therefore, high-frequency stimulation in HPC may be a useful tool to better understand how to prevent NMDAr hypofunction effects on synaptic plasticity and oscillatory coordination in corticolimbic circuits. The hippocampal-prefrontal cortex (HPC-PFC) monosynaptic pathway is implicated in cognitive functions, such as working memory, decision making, and spatial-temporal processing 1,2. Dysfunctional connectivity within HPC-PFC circuits is associated with the pathophysiology and genetic predisposition to schizophrenia 3-5. In schizophrenia, HPC-PFC connectivity is decreased during working memory tasks and increased in resting state 5-7. Such effects may be mediated, at least in part, by N-methyl-D-aspartate receptor (NMDAr). NMDAr binding is reduced in schizophrenic patients in both HPC and PFC, and administration of an NMDAr antagonist, such as ketamine, can induce psychotic symptoms in healthy patients and an increase in resting-state HPC-PFC connectivity 8-10. This NMDAr hypofunction also affects synaptic plasticity, inducing impairments in critical circuits, such as HPC-PFC, promoting cognitive symptoms by pathological neural activity 11-13. However, the relationship between synaptic plasticity in HPC-PFC circuits and schizophrenia is not fully understood.

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“…It is believed that SWR power is associated with higher fidelity replay of past experiences and of place cell trajectories (Carr et al, 2012 ). In line with this notion, disruption of SWRs and/or gamma oscillation in the HPC-EC of experimental animals and humans causes severe memory impairment (Le Van Quyen et al, 2010 ; Jadav et al, 2012 ; Fernandez-Ruiz et al, 2019 , 2021 ; Hollnagel et al, 2019 ; Jones et al, 2019 ; Mendes et al, 2019 ).…”

Section: Introductionmentioning

confidence: 90%

Normal and Abnormal Sharp Wave Ripples in the Hippocampal-Entorhinal Cortex System: Implications for Memory Consolidation, Alzheimer's Disease, and Temporal Lobe Epilepsy

Zhen

Guo

et al. 2021

Front. Aging Neurosci.

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The appearance of hippocampal sharp wave ripples (SWRs) is an electrophysiological biomarker for episodic memory encoding and behavioral planning. Disturbed SWRs are considered a sign of neural network dysfunction that may provide insights into the structural connectivity changes associated with cognitive impairment in early-stage Alzheimer's disease (AD) and temporal lobe epilepsy (TLE). SWRs originating from hippocampus have been extensively studied during spatial navigation in rodents, and more recent studies have investigated SWRs in the hippocampal-entorhinal cortex (HPC-EC) system during a variety of other memory-guided behaviors. Understanding how SWR disruption impairs memory function, especially episodic memory, could aid in the development of more efficacious therapeutics for AD and TLE. In this review, we first provide an overview of the reciprocal association between AD and TLE, and then focus on the functions of HPC-EC system SWRs in episodic memory consolidation. It is posited that these waveforms reflect rapid network interactions among excitatory projection neurons and local interneurons and that these waves may contribute to synaptic plasticity underlying memory consolidation. Further, SWRs appear altered or ectopic in AD and TLE. These waveforms may thus provide clues to understanding disease pathogenesis and may even serve as biomarkers for early-stage disease progression and treatment response.

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Hijacking of hippocampal–cortical oscillatory coupling during sleep in temporal lobe epilepsy

Cited by 13 publications

References 38 publications

Sleep Disruption in Epilepsy: Ictal and Interictal Epileptic Activity Matter

Sleep Disruption in Epilepsy: Ictal and Interictal Epileptic Activity Matter

Long-term potentiation prevents ketamine-induced aberrant neurophysiological dynamics in the hippocampus-prefrontal cortex pathway in vivo

Normal and Abnormal Sharp Wave Ripples in the Hippocampal-Entorhinal Cortex System: Implications for Memory Consolidation, Alzheimer's Disease, and Temporal Lobe Epilepsy

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