Selective suppression of hippocampal ripples impairs spatial memory

Girardeau, Gabrielle; Benchenane, Karim; Wiener, Sidney I.; Buzsáki, György; Zugaro, Michaël

doi:10.1038/nn.2384

Cited by 1,315 publications

(1,192 citation statements)

References 14 publications

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“…Importantly, this replay seems to coincide with the sharp wave ripples that originate in the hippocampus and are characteristic of SWS. These have been shown to be important for spatial learning in rats, with disruption of sharp wave ripples resulting in severely impaired consolidation [63,64], Figure I.…”

Section: Offline Memory Replaymentioning

confidence: 99%

Overlapping memory replay during sleep builds cognitive schemata

Lewis

Durrant

2011

Trends in Cognitive Sciences

458

437

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Sleep enhances integration across multiple stimuli, abstraction of general rules, insight into hidden solutions and false memory formation. Newly learned information is better assimilated if compatible with an existing cognitive framework or schema. This article proposes a mechanism by which the reactivation of newly learned memories during sleep could actively underpin both schema formation and the addition of new knowledge to existing schemata. Under this model, the overlapping replay of related memories selectively strengthens shared elements. Repeated reactivation of memories in different combinations progressively builds schematic representations of the relationships between stimuli. We argue that this selective strengthening forms the basis of cognitive abstraction, and explain how it facilitates insight and false memory formation.What's the gist? I do not remember many details about childhood birthday parties. There was one when we played blind man's bluff, and another with cucumber sandwiches, but in general these affairs blur together under the broad heading of birthdays. About this category I have much information: I know the parties involved hordes of children, that there were presents and invariably a cake. However, which birthday belonged to whom, and exactly what was done there escapes me. This is unsurprising as chronologically old memories rarely include clear episodic details but these aspects of a situation or memory type that are repeated again and again are normally recalled with ease. Central shared concepts of this type can be thought of as the 'gist' (see Glossary), or essential features, of a set of memories, and taken together can form a cognitive framework of expectations or schema (Box 1). This article proposes a physiological mechanism by which memory replay during sleep could be responsible for the abstraction of gist information from newly encoded memories to form cognitive schemata.Recent research has shown that sleep facilitates abstraction of gist information [1][2][3][4][5] as well as integration across multiple memories [6][7][8], insight into hidden solutions [9], and even the ability to make creative connections between distantly related ideas and concepts [10]. These findings build upon a strong body of work demonstrating that sleep plays a crucial role in memory consolidation (for reviews [11][12][13]), as well as a highly influential model of how memories are re-organised and strengthened by replay during slow wave sleep (SWS) (see [11,12,[14][15][16][17] and Box 2). This model elegantly explains how the specific physiology of SWS, in combination with the replay of memories that has been observed in both rats and humans during this sleep stage (Box 3), could assist consolidation by transferring memories from a short-term store in the hippocampus to longer term cortical representations. Importantly, however, this model cannot presently explain why sleep is beneficial for gist extraction, insight or the formation of false memories.A separate line of research investigating th...

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Section: Offline Memory Replaymentioning

confidence: 99%

Overlapping memory replay during sleep builds cognitive schemata

Lewis

Durrant

2011

Trends in Cognitive Sciences

458

437

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“…Memory consolidation is thought to involve post-encoding reactivation of the activity patterns present during initial experience (activity replay) (Girardeau et al, 2009;Dupret et al, 2010). The frequency of activity replay decreases after the learning experience; replay is most frequent in the minutes following an experience (Tatsuno et al, 2006) but may persist for 18-24 h (Kudrimoti et al, 1999).…”

Section: Ic++ Silencing Of Creb-overexpressing Dg Neurons Shortly Aftmentioning

confidence: 99%

“…This result and other similar studies (Liu et al, 2012;Ramirez et al, 2013) identify neurons allocated to an engram. However, post-learning processes, presumably in neurons allocated to the engram, are thought to be important for successful memory consolidation (Marr, 1971;Buzsáki, 1989;Wilson and McNaughton, 1994;Girardeau et al, 2009;Ego-Stengel and Wilson, 2010;Carr et al, 2011). In vivo recording studies show that the precise patterns of event-induced neuronal activity may be subsequently replayed offline, during sleep (Skaggs and McNaughton, 1996;Ji and Wilson, 2007), or quiet wakeful periods (Carr et al, 2011).…”

Section: Inhibition Of a Dg Fear Engram Shortly After Training Disrupmentioning

confidence: 99%

Neuronal Allocation to a Hippocampal Engram

Park

Kramer

Mercaldo

et al. 2016

Neuropsychopharmacol

156

113

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The dentate gyrus (DG) is important for encoding contextual memories, but little is known about how a population of DG neurons comes to encode and support a particular memory. One possibility is that recruitment into an engram depends on a neuron's excitability. Here, we manipulated excitability by overexpressing CREB in a random population of DG neurons and examined whether this biased their recruitment to an engram supporting a contextual fear memory. To directly assess whether neurons overexpressing CREB at the time of training became critical components of the engram, we examined memory expression while the activity of these neurons was silenced. Chemogenetically (hM4Di, an inhibitory DREADD receptor) or optogenetically (iC++, a light-activated chloride channel) silencing the small number of CREB-overexpressing DG neurons attenuated memory expression, whereas silencing a similar number of random neurons not overexpressing CREB at the time of training did not. As post-encoding reactivation of the activity patterns present during initial experience is thought to be important in memory consolidation, we investigated whether post-training silencing of neurons allocated to an engram disrupted subsequent memory expression. We found that silencing neurons 5 min (but not 24 h) following training disrupted memory expression. Together these results indicate that the rules of neuronal allocation to an engram originally described in the lateral amygdala are followed in different brain regions including DG, and moreover, that disrupting the post-training activity pattern of these neurons prevents memory consolidation.

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“…More recently, cortical inhibitory networks have also been proposed to play a critical role in the generation of faster activities that include oscillations in the low (i.e, beta-gamma oscillations at 20-80 Hz) and high frequency range (>80 Hz, so called ripples) (Buzsáki et al, 1992). Interestingly, both beta-gamma rhythms and ripples occurring in cortical areas (Gray et al, 1989;Murthy and Fetz, 1992;Singer and Gray, 1995), including those of the limbic system Chrobak and Buzsáki, 1998;Csicsvari et al, 1999Csicsvari et al, , 2003, have been implicated in higher brain processes such as attention, sensorimotor integration, consciousness, learning and memory (Girardeau et al, 2009;Montgomery and Buzsáki, 2007). Therefore, it has been suggested that these oscillatory rhythms represent the basic neuronal processing state of the brain (Basar et al, 1999).…”

Section: Role Of Gaba a Receptors In Neuronal Network Oscillationsmentioning

confidence: 99%

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

Avoli¹,

Curtis²

2011

Progress in Neurobiology

228

253

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GABA is the main inhibitory neurotransmitter in the adult forebrain, where it activates ionotropic type A and metabotropic type B receptors. Early studies have shown that GABA A receptormediated inhibition controls neuronal excitability and thus the occurrence of seizures. However, more complex, and at times unexpected, mechanisms of GABAergic signaling have been identified during epileptiform discharges over the last few years. Here, we will review experimental data that point at the paradoxical role played by GABA A receptor-mediated mechanisms in synchronizing neuronal networks, and in particular those of limbic structures such as the hippocampus, the entorhinal and perirhinal cortices, or the amygdala. After having summarized the fundamental characteristics of GABA A receptor-mediated mechanisms, we will analyze their role in the generation of network oscillations and their contribution to epileptiform synchronization. Whether and how GABA A receptors influence the interaction between limbic networks leading to ictogenesis will be also reviewed. Finally, we will consider the role of altered inhibition in the human epileptic brain along with the ability of GABA A receptor-mediated conductances to generate synchronous depolarizing events that may lead to ictogenesis in human epileptic disorders as well.

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Selective suppression of hippocampal ripples impairs spatial memory

Cited by 1,315 publications

References 14 publications

Overlapping memory replay during sleep builds cognitive schemata

Overlapping memory replay during sleep builds cognitive schemata

Neuronal Allocation to a Hippocampal Engram

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

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