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

Author(s)

Mendes, Renan Augusto Viana ^[1] ; Zacharias, Leonardo Rakauskas ^[2] ; Ruggiero, Rafael Naime ^[2] ; Leite, Joao Pereira ^[2] ; Moraes, Marcio Flavio Dutra ^[1] ; Lopes-Aguiar, Cleiton ^[1]

Affiliation

^[1] Univ Fed Minas Gerais, Inst Ciencias Biol, Dept Fisiol & Biofis, Nucleo Neurociencias, Belo Horizonte, MG - Brazil

^[2] Univ Sao Paulo, Fac Med Ribeirao Preto, Dept Neurociencias & Ciencias Comportamento, Ribeirao Preto - Brazil

• Document type: Journal article
• Source: Epilepsy & Behavior; v. 121, n. B AUG 2021.
• Web of Science Citations: 1

Abstract

Memory impairment is the most common cognitive deficit in patients with temporal lobe epilepsy (TLE). This type of epilepsy is currently regarded as a network disease because of its brain-wide alterations in functional connectivity between temporal and extra-temporal regions. In patients with TLE, network dysfunctions can be observed during ictal states, but are also described interictally during rest or sleep. Here, we examined the available literature supporting the hypothesis that hippocampal \& ndash;cortical coupling during sleep is hijacked in TLE. First, we look at studies showing that the coordination between hippocampal sharp-wave ripples (100 \& ndash;200 Hz), corticothalamic spindles (9 \& ndash;16 Hz), and cortical delta waves (1 \& ndash;4 Hz) during nonrapid eye movement (NREM) sleep is critical for spatial memory consolidation. Then, we reviewed studies showing that animal models of TLE display precise coordination between hippocampal interictal epileptiform discharges (IEDs) and spindle oscillations in the prefrontal cortex. This aberrant oscillatory coupling seems to surpass the physiological ripple \& ndash;delta-spindle coordination, which could underlie memory consolidation impairments. We also discuss the role of rapid eye movement (REM) sleep for local synaptic plasticity and memory. Sleep episodes of REM provide windows of opportunity for reactivation of expression of immediate early genes (i.e., zif-268 and Arc). Besides, hippocampal theta oscillations during REM sleep seem to be critical for memory consolidation of novel object place recognition task. However, it is still unclear which extend this particular phase of sleep is affected in TLE. In this context, we show some preliminary results from our group, suggesting that hippocampal theta \& ndash;gamma phase \& ndash;amplitude coupling is exacerbated during REM in a model of basolateral amygdala fast kindling. In conclusion, there is an increasing body of evidence suggesting that circuits responsible for memory consolidation during sleep seem to be gradually coopted and degraded in TLE. This article is part of the Special Issue \& ldquo;NEWroscience 2018{''} (c) 2019 Elsevier Inc. All rights reserved. (AU)

• FAPESP's process: 18/02303-4 - Study of the meso-cortico-limbic connectivity in animals submitted to early-life Status epilepticus and its relationship with psychiatric comorbidities
• Grantee: Rafael Naime Ruggiero
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 16/17882-4 - Drug-resistant epilepsies: diagnostic challenges, associated comorbidities and new experimental approaches
• Grantee: João Pereira Leite
• Support Opportunities: Research Projects - Thematic Grants