Hippocampal ripples down-regulate synapses

Abstract

The specific effects of sleep on synaptic plasticity remain unclear. We report that mouse hippocampal sharp-wave ripple oscillations serve as intrinsic events that trigger long-lasting synaptic depression. Silencing of sharp-wave ripples during slow-wave states prevented the spontaneous down-regulation of net synaptic weights and impaired the learning of new memories. The synaptic down-regulation was dependent on the -methyl-d-aspartate receptor and selective for a specific input pathway. Thus, our findings are consistent with the role of slow-wave states in refining memory engrams by reducing recent memory-irrelevant neuronal activity and suggest a previously unrecognized function for sharp-wave ripples.

Remembering rewarding futures: A simulation‐selection model of the hippocampus

“…It is currently controversial whether hippocampal synapses are potentiated or exclusively depressed during SWRs (Bukalo, Campanac, Hoffman, & Fields, ; Buzsaki, ; Buzsaki, Haas, & Anderson, ; Colgin, Kubota, Jia, Rex, & Lynch, ; King, Henze, Leinekugel, & Buzsaki, ; Leonard, Mcnaughton, & Barnes, ; Norimoto et al, ; Sadowski, Jones, & Mellor, ; Tononi & Cirelli, ). Nevertheless, both synaptic potentiation and depression have been proposed as mechanisms for memory consolidation (Bukalo et al, ; Norimoto et al, ; Sadowski et al, ; Tononi & Cirelli, ). Those hippocampal synapses supporting frequently replayed rewarding sequences may be further strengthened and/or other synapses are weakened during SWRs, so that relative strengths of frequently replayed sequences are enhanced.…”

Place cell map genesis via competitive learning and conjunctive coding in the dentate gyrus

“…Periods of rest between treadmill running sessions were likely essential to regenerate the network potency for plasticity, as the place field emergence rate progressively decreased across trials within each session ( Figure 4D). Synaptic normalization, especially, might require sleep and sharpwave-ripple oscillations to develop (Norimoto et al, 2018;Vyazovskiy et al, 2008), considering the relatively slow rate of synaptic downscaling observed in vitro (Royer an Paré, 2003).…”

CA3 place cells that represent a novel waking experience are preferentially reactivated during sharp wave-ripples in subsequent sleep

“…On the other hand, a second possible way to selectively increase the relative strength of synaptic connections underlying newly encoded memories is to weaken synaptic connections between neurons that do not store novel information. Several studies have suggested that SWRs can weaken synaptic strength (Colgin et al, 2004; Bukalo et al, 2013; Norimoto et al, 2018). In particular, a recent study reported that silencing SWR-related neuronal activity during NREM sleep prevents spontaneous weakening of synapses and impairs subsequent learning of new memories (Norimoto et al, 2018).…”

“…Several studies have suggested that SWRs can weaken synaptic strength (Colgin et al, 2004; Bukalo et al, 2013; Norimoto et al, 2018). In particular, a recent study reported that silencing SWR-related neuronal activity during NREM sleep prevents spontaneous weakening of synapses and impairs subsequent learning of new memories (Norimoto et al, 2018). This study further showed that place cells active in a novel environment maintained their firing rates during SWRs across NREM sleep while other hippocampal cells’ firing rates gradually declined during SWRs across the course of NREM sleep.…”