Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval

By Margaret F. Carr, Shantanu P. Jadhav, Loren M. Frank. 2011

879 citations recorded by the source corpus.

The hippocampus is required for the encoding, consolidation and retrieval of event memories. Although the neural mechanisms that underlie these processes are only partially understood, a series of recent papers point to awake memory replay as a potential contributor to both consolidation and retrieval. Replay is the sequential reactivation of hippocampal place cells that represent previously experienced behavioral trajectories and occurs frequently in the awake state, particularly during periods of relative immobility. Awake replay may reflect trajectories through either the current environment or previously visited environments that are spatially remote. The repetition of learned sequences on a compressed time scale is well suited to promote memory consolidation in distributed circuits beyond the hippocampus, suggesting that consolidation occurs in both the awake and sleeping animal. Moreover, sensory information can influence the content of awake replay, suggesting a role for awake replay in memory retrieval.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neuroscience

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Citations in the corpus

A Comprehensive Survey of Continual Learning: Theory, Method and Application (2023, background): “2 seconds) [52], [84], [227], which potentially improves resource efficiency.”
Lifelong Learning of Spatiotemporal Representations With Dual-Memory Recurrent Self-Organization (2018, background): “This is consistent with biological evidence suggesting that the reactivation of hippocampal representations and their frequent replay to the neocortex are crucial for memory consolidation and retrieval (see Carr et al., 2011 for a review).”
Selective Experience Replay for Lifelong Learning (2018, background): “Research shows that blocking re-play 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).”
Memory Replay with Data Compression for Continual Learning (2022, positive): “Different from “artificial” memory replay in DNNs, a significant feature of biological memory is to encode the old experiences in a highly compressed form and replay them to overcome catastrophic forgetting (McClelland, 2013; Davidson et al., 2009; Carr et al., 2011).”
Lifelong Generative Modeling (2017, background): “These replays are necessary for better planning [53] and memory consolidation [16].”
Neurogenesis deep learning: Extending deep networks to accommodate new classes (2016, background): “Class conditional sampling from trained networks has biological inspiration [21]-[24] as well as historical and artificial neural network implementations [25]-[28].”
About sleep's role in memory. (2013, background): “Why does the consolidation of memory have to take place during sleep? The hypotheses that sleep serves memory consolidation is conceptually rooted in the standard two-stage memory system which is currently the most influential model of human memory, and has been developed as a solution to several ke”
Memory engrams: Recalling the past and imagining the future (2020, background): “Post-encoding reactivation or replay of hippocampal place cell firing, especially during slow-wave sleep (SWS) (87, 88), is thought to be important for memory consolidation (89-92).”
What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated. (2016, neutral): “Instead, mounting evidence suggests that replay may be biased towards rewarding events [59,76].”
Replay Comes of Age. (2017, background): “Several recent reviews have covered similar ground, including some shorter reviews (Carr et al. 2011, O’Neill et al. 2010) and a very comprehensive review of related and overlapping phenomena in the local hippocampal electroencelphalogram (EEG) (Buzsaki 2015).”
Episodic-like memory trace in awake replay of hippocampal place cell activity sequences (2015, background): “…therefore proposed a unified interpretation in which replays provide information on possible upcoming paths to downstream brain structures such as the prefrontal cortex and nucleus accumbens, which can assess the value of different paths and make a decision about future actions (Carr et al., 2011).”
Awake reactivation of emotional memory traces through hippocampal-neocortical interactions (2016, neutral): “Indeed, electrophysiological studies in rodents show that firing patterns of hippocampal place cells present during encoding reoccur during sleep (Wilson and McNaughton, 1994) and awake states (Carr et al., 2011).”
Gamma frequency entrainment attenuates amyloid load and modifies microglia (2016, neutral): “1b, left); and quiescent behaviour, when sharp-wave rip-ples (SWRs) occur 15,16 (Extended Data Fig.”
The content of hippocampal “replay” (2018, background): “…Buzs aki, 2016), raising the intriguing possibility that forward replay itself can serve two purposes depending on the behavioral state of the animal (Diekelmann et al., 2011): memory retrieval during the awake state and memory consolidation during sleep (Carr et al., 2011; Lewis & Durrant, 2011).”
Self-Net: Lifelong Learning via Continual Self-Modeling (2018, background): “Speciﬁcally, there is evidence that the hippocampus uses experience replay (ER) to perform this knowledge consolidation (Carr et al., 2011; Kumaran et al., 2016).”