Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat

By Valerie Ego-Stengel, M. A. Wilson. 2009

771 citations recorded by the source corpus.

The hippocampus plays a key role in the acquisition of new memories for places and events. Evidence suggests that the consolidation of these memories is enhanced during sleep. At the neuronal level, reactivation of awake experience in the hippocampus during sharp‐wave ripple events, characteristic of slow‐wave sleep, has been proposed as a neural mechanism for sleep‐dependent memory consolidation. However, a causal relation between sleep reactivation and memory consolidation has not been established. Here we show that disrupting neuronal activity during ripple events impairs spatial learning. We trained rats daily in two identical spatial navigation tasks followed each by a 1‐hour rest period. After one of the tasks, stimulation of hippocampal afferents selectively disrupted neuronal activity associated with ripple events without changing the sleep‐wake structure. Rats learned the control task significantly faster than the task followed by rest stimulation, indicating that interfering with hippocampal processing during sleep led to decreased learning. © 2009 Wiley‐Liss, Inc.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Generalization Through the Recurrent Interaction of Episodic Memories (2012, methodology): “We relate our model to spontaneously generated neural activity in the hippocampus during resting states such as slow wave sleep (Buzsáki, 1989; Ego-Stengel & Wilson, 2010; Foster & Wilson, 2006; Girardeau et al., 2009; Gupta et al., 2010; Lee & Wilson, 2002; McClelland et al., 1995; Wilson &…”
Selective Experience Replay for Lifelong Learning (2018, background): “Research shows that blocking replay disrupts learning (Girardeau et al. 2009; Ego-Stengel and Wilson 2010) and some suggest that replay is a necessary component of memory consolidation (Carr, Jadhav, and Frank 2011).”
Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, positive): “Causal evidence for a role of awake replay in memory consolidation is still lacking, but two recent studies have used real-time disruption of SWRs during sleep to demonstrate the link between hippocampal SWRs during sleep and learnin”
Hippocampal Replay is Not a Simple Function of Experience (2010, background): “…learning (Hoffman and McNaughton, 2002; Euston et al., 2007; Ji and Wilson, 2007) as well as transfers of dependence (Squire, 1987; Maviel et al., 2004) and learning changes from disruption of SWRs (Girardeau et al., 2009; Ego-Stengel and Wilson, 2010; J.C. Jackson et al., 2009, Soc.”
About sleep's role in memory. (2013, background): “Two recent studies in rats demonstrated a causal role of SW-Rs in memory consolidation (340, 458).”
Online Continual Learning from Imbalanced Data (2020, background): “Research in the ﬁeld of neuroscience has shown that replay is also present in living beings and is connected to the process of memory consolidation (Girardeau et al., 2009; Ego-Stengel & Wilson, 2010).”
Memory engrams: Recalling the past and imagining the future (2020, background): “Disrupting either sharp-wave ripple– spindle coupling (115, 116) or sharp-wave ripple– associated replay of hippocampal place cells (104, 105, 117, 118) impairs memory recall.”
The restless engram: consolidations never end. (2012, background): “Girardeau et al. (2009) and Ego-Stengel & Wilson (2010) stimulated the hippocampus to selectively disrupt SWR activity in maze-trained rats.”
Neuromodulation of brain states. (2012, positive): “Selective interruption of hippocampal ripple events during wakefulness impairs spatial learning (Jadhav et al., 2012), similar to the effect of ripple disruption during sleep (Ego-Stengel and Wilson, 2010; Girardeau et al., 2009).”
What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated. (2016, positive): “A causal role for replay is supported by studies showing that the disruption of ripples in the hippocampus produces a signi ﬁ cant impairment in systems-level consolidation in rats [67 – 69].”
Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory (2014, background): “…© 2014 the authors 0270-6474/14/345134-09$15.00/0 ruption of hippocampal sharp-wave/ripple activity during posttraining sleep can impair memory consolidation (Ego-Stengel and Wilson, 2010), whereas enhancement of cortical slow-waves can enhance memory consolidation (Marshall et al., 2006).”
Cellular and Systems Consolidation of Declarative Memory (2017, background): “…2009; Ramanathan et al. 2015; Yang et al. 2014) and disrupting sharp-wave-ripples and thus replay during sleep leads to a deficit in hippocampal led consolidation (Ego-Stengel and Wilson 2010; Girardeau et al. 2009), providing further evidence for the importance of sleep in systems consolidation.”
The content of hippocampal “replay” (2018, background): “…slow-wave sleep, quiet rest, grooming, and eating/drinking (Buzs aki, 1986, 2015), and disruption in their expression results in significant memory impairments (Ego-Stengel & Wilson, 2010; Girardeau et al., 2009; Jadhav et al., 2012; Nakashiba et al., 2009; Nokia et al., 2012; Wang et al., 2015a).”