Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep

Euston, David R.; Tatsuno, Masami; McNaughton, Bruce L.

doi:10.1126/science.1148979

Cited by 490 publications

(516 citation statements)

References 29 publications

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“…This mechanism is compelling in its simplicity and in its effortless fit to the literature on reactivation of memories in rats [21,22] and humans [23][24][25][26], as well as to research on concept formation [27]. It explains why newly learned material becomes increasingly easy to integrate and remember as a conceptual schema takes shape [18,19].…”

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confidence: 99%

Overlapping memory replay during sleep builds cognitive schemata

Lewis

Durrant

2011

Trends in Cognitive Sciences

443

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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confidence: 99%

Overlapping memory replay during sleep builds cognitive schemata

Lewis

Durrant

2011

Trends in Cognitive Sciences

443

437

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“…These functions likely depend on reciprocal interactions with the hippocampus (13,14), an area that has a well-established role in spatial and contextual processing (15)(16)(17)(18)(19)(20). Through the connection from the CA1 region, the hippocampus has multiple profound effects on mPFC neurons (21)(22)(23)(24)(25)(26)(27)(28), and it has been proposed that during spatial navigation the mPFC may work in concert with the hippocampus to encode goal locations and aid in route planning (29,30). However, the spatial representations formed by the mPFC are different from those formed by the hippocampus: mPFC neurons do not seem to have clear place fields and presumably do not form the same sort of spatial map that would inform the animal precisely where it is within an environmental context (31)(32)(33)(34).…”

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confidence: 99%

Contextual encoding by ensembles of medial prefrontal cortex neurons

Hyman

Balaguer‐Ballester

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

209

204

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Contextual representations serve to guide many aspects of behavior and influence the way stimuli or actions are encoded and interpreted. The medial prefrontal cortex (mPFC), including the anterior cingulate subregion, has been implicated in contextual encoding, yet the nature of contextual representations formed by the mPFC is unclear. Using multiple single-unit tetrode recordings in rats, we found that different activity patterns emerged in mPFC ensembles when animals moved between different environmental contexts. These differences in activity patterns were significantly larger than those observed for hippocampal ensembles. Whereas ≈11% of mPFC cells consistently preferred one environment over the other across multiple exposures to the same environments, optimal decoding (prediction) of the environmental setting occurred when the activity of up to ≈50% of all mPFC neurons was taken into account. On the other hand, population activity patterns were not identical upon repeated exposures to the very same environment. This was partly because the state of mPFC ensembles seemed to systematically shift with time, such that we could sometimes predict the change in ensemble state upon later reentry into one environment according to linear extrapolation from the time-dependent shifts observed during the first exposure. We also observed that many strongly action-selective mPFC neurons exhibited a significant degree of context-dependent modulation. These results highlight potential differences in contextual encoding schemes by the mPFC and hippocampus and suggest that the mPFC forms rich contextual representations that take into account not only sensory cues but also actions and time.electrophysiological recordings | population analysis | temporal encoding M any aspects of behavior are contextually dependent. Contexts can be abstract, as in the case of human language, or can be more concrete and be defined by the constellation of spatial and sensory stimuli surrounding an individual. Contextual representations can form quickly and tend to remain stable despite local variations in perspective (1). Context can also help to inform the subject about potential changes in the meaning of stimuli and actions. The medial prefrontal cortex (mPFC) is involved in various forms of cognition that depend on spatial and contextual information, including context-based cognitive tasks (2-4), contextual fear conditioning (5), and context-induced drug relapse (6-8), and is believed to be an important node in the "context" network (1, 9-12). These functions likely depend on reciprocal interactions with the hippocampus (13, 14), an area that has a well-established role in spatial and contextual processing (15)(16)(17)(18)(19)(20). Through the connection from the CA1 region, the hippocampus has multiple profound effects on mPFC neurons (21-28), and it has been proposed that during spatial navigation the mPFC may work in concert with the hippocampus to encode goal locations and aid in route planning (29,30). However, the spatial representations ...

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“…Although reactivation had originally been reported in the hippocampus as a mechanism of memory consolidation (12)(13)(14), it may constitute a fundamental property of neural ensembles in many brain areas. Indeed, in addition to hippocampus, reactivation has been reported in rat prefrontal cortex (15)(16)(17), motor and somatosensory cortex during quiescent awake states (18), rat primary visual cortex (V1) during slow-wave sleep (19), and rat and cat V1 immediately after stimulus presentation during anesthesia (20)(21)(22).…”

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confidence: 99%

Image sequence reactivation in awake V4 networks

Eagleman

Dragoi

2012

Proc. Natl. Acad. Sci. U.S.A.

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In the absence of sensory input, neuronal networks are far from being silent. Whether spontaneous changes in ongoing activity reflect previous sensory experience or stochastic fluctuations in brain activity is not well understood. Here we describe reactivation of stimulusevoked activity in awake visual cortical networks. We found that continuous exposure to randomly flashed image sequences induces reactivation in macaque V4 cortical networks in the absence of visual stimulation. This reactivation of previously evoked activity is stimulusspecific, occurs only in the same temporal order as the original response, and strengthens with increased stimulus exposures. Importantly, cells exhibiting significant reactivation carry more information about the stimulus than cells that do not reactivate. These results demonstrate a surprising degree of experience-dependent plasticity in visual cortical networks as a result of repeated exposure to unattended information. We suggest that awake reactivation in visual cortex may underlie perceptual learning by passive stimulus exposure.electrophysiology | monkey

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Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep

Cited by 490 publications

References 29 publications

Overlapping memory replay during sleep builds cognitive schemata

Overlapping memory replay during sleep builds cognitive schemata

Contextual encoding by ensembles of medial prefrontal cortex neurons

Image sequence reactivation in awake V4 networks

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