Soluble amyloid beta oligomers block the learning-induced increase in hippocampal sharp wave-ripple rate and impair spatial memory formation - Archive ouverte HAL Accéder directement au contenu
Article Dans Une Revue Scientific Reports Année : 2016

Soluble amyloid beta oligomers block the learning-induced increase in hippocampal sharp wave-ripple rate and impair spatial memory formation

Résumé

Post-learning hippocampal sharp wave-ripples (SWRs) generated during slow wave sleep are thought to play a crucial role in memory formation. While in Alzheimer's disease, abnormal hippocampal oscillations have been reported, the functional contribution of SWRs to the typically observed spatial memory impairments remains unclear. These impairments have been related to degenerative synaptic changes produced by soluble amyloid beta oligomers (Aβos) which, surprisingly, seem to spare the SWR dynamics during routine behavior. To unravel a potential effect of Aβos on SWRs in cognitively-challenged animals, we submitted vehicle-and Aβo-injected mice to spatial recognition memory testing. While capable of forming short-term recognition memory, Aβ mice exhibited faster forgetting, suggesting successful encoding but an inability to adequately stabilize and/or retrieve previously acquired information. Without prior cognitive requirements, similar properties of SWRs were observed in both groups. In contrast, when cognitively challenged, the post-encoding and-recognition peaks in SWR occurrence observed in controls were abolished in Aβ mice, indicating impaired hippocampal processing of spatial information. These results point to a crucial involvement of SWRs in spatial memory formation and identify the Aβ-induced impairment in SWRs dynamics as a disruptive mechanism responsible for the spatial memory deficits associated with Alzheimer's disease. Information processing and memory formation in rodents have been reported to be accompanied by an array of hippocampal field potential oscillations that are important functionally. For instance, theta oscillations occur during active behavior and rapid eye movement (REM) sleep and have been suggested to provide the temporal frame for the encoding of information 1. Gamma oscillations triggered during exploratory behavior are thought to be involved in memory acquisition 2 and their synchronization contributes to successful execution of working memory 3. During slow wave sleep (SWS) that follows learning, hippocampal circuits consistently increase the occurrence rates of sharp wave-ripples (SWRs) which typically recur at 0.4 to 1 Hz 4,5. Importantly, upon occurrence of SWRs, ensembles of hippocampal place cells can replay in faster timescales their sequential activity triggered during a previous learning episode, suggesting an essential role for SWRs in driving memory consolidation processes and subsequent long-term stabilization of newly acquired spatial memory traces 6. When such SWRs are experimentally disrupted, it causes memory deficits in hippocampus-dependent memory tasks 7 , further suggesting that abnormal hippocampal rhythmic activity can interfere with hippocampal information processing, a dysfunctional pattern also observed in pathological conditions such as Alzheimer's disease 8 (AD). The cognitive impairments associated with AD are related to degenerative synaptic changes produced by the presence of soluble amyloid beta proteins (Aβ s) in vulnerable brain regions such as the hippocampus considered

Domaines

Neurobiologie
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Dates et versions

hal-01284761 , version 1 (08-03-2016)

Identifiants

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Olivier Nicole, Senka Hadzibegovic, Judyta Gajda, Bruno Bontempi, Tiaza Bem, et al.. Soluble amyloid beta oligomers block the learning-induced increase in hippocampal sharp wave-ripple rate and impair spatial memory formation. Scientific Reports, 2016, 6, pp.22728. ⟨10.1038/srep22728⟩. ⟨hal-01284761⟩

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