Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval
Open accessAbstract
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.
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There is evidence that humans do repeat some of the information they process (e.g., in memory replay).
“there is evidence that humans do repeat some of the information they process (e.g., in memory replay, Carr et al., 2011).”
From Findings of the BabyLM Challenge: Sample-Efficient Pretraining on Developmentally Plausible Corpora (2023) · cites this paper as Carr et al., 2011
The ‘Awake replay of the local environment’ section (page unavailable) reports that animals repeatedly replayed sequences representing previously experienced trajectories. This supports the memory-replay example, but the passage concerns animals, not evidence that humans do this. (LLM, conf=0.87)
Experimental — accuracy not yet measuredAwake memory reactivations have been shown to enhance subsequent recall performance.
“awake memory reactivations have been shown to enhance subsequent recall performance.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [151]
In “Linking awake replay and memory consolidation” (page unavailable), the review reports that the strength of awake reactivation predicted subsequent memory-task performance in animals. That supports an association, but not the claim that reactivation was shown to enhance subsequent recall performance: the passage does not establish a causal improvement or identify a recall measure. (LLM, conf=0.86)
Experimental — accuracy not yet measured
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Cites
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
Bi, G.-Q., & Poo, M.-M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10464.1998 · Cited by 4,744 · see citing works
Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564 · see citing works
The Medial Temporal Lobe Memory System
Squire, L. R., & Zola-Morgan, S. (1991) · Science · doi:10.1126/science.1896849 · Cited by 3,282 · see citing works
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
Phase relationship between hippocampal place units and the EEG theta rhythm
O'Keefe, J. M., & Recce, M. L. (1993) · Hippocampus · doi:10.1002/hipo.450030307 · Cited by 2,561 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
The locus coeruleus and noradrenergic modulation of cognition
Sara, S. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2573 · Cited by 1,848 · see citing works
Reverse replay of behavioural sequences in hippocampal place cells during the awake state
Foster, D. J., & Wilson, M. A. (2006) · Nature · doi:10.1038/nature04587 · Cited by 1,727 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
The role of acetylcholine in learning and memory
Hasselmo, M. E. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.09.002 · Cited by 1,693 · see citing works
The Neurobiology of Consolidations, Or, How Stable is the Engram?
Dudai, Y. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.142050 · Cited by 1,671 · see citing works
Selective suppression of hippocampal ripples impairs spatial memory
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2384 · Cited by 1,560 · see citing works
Memory, amnesia, and the hippocampal system
(1994) · Choice Reviews Online · doi:10.5860/choice.31-5148 · Cited by 1,533 · see citing works
Cellular bases of hippocampal EEG in the behaving rat
Buzsáki, G., Leung Lai-Wo, S., & Vanderwolf, C. H. (1983) · Brain Research Reviews · doi:10.1016/0165-0173(83)90037-1 · Cited by 1,397 · see citing works
Hippocampal synaptic enhancement and information storage within a distributed memory system
McNaughton, B. L., & Morris, R. G. M. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90011-7 · Cited by 1,304 · see citing works
Memory of sequential experience in the hippocampus during slow wave sleep
Lee, A. K., & Wilson, M. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)01096-6 · Cited by 1,296 · see citing works
Schemas and Memory Consolidation.
Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., Witter, M. P., & Morris, R. G. M. (2007) · Science · doi:10.1126/science.1135935 · Cited by 1,244 · see citing works
Forward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205 · see citing works
Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience
Skaggs, W. E., & McNaughton, B. L. (1996) · Science · doi:10.1126/science.271.5257.1870 · Cited by 1,173 · see citing works
Memory consolidation and the medial temporal lobe: a simple network model.
Alvarez, P., & Squire, L. R. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.7041 · Cited by 1,054 · see citing works
Coordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052 · see citing works
Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task
Jones, M. W., & Wilson, M. A. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030402 · Cited by 1,036 · see citing works
From Conditioning to Conscious Recollection
Eichenbaum, H., & Cohen, N. J. (2004) · doi:10.1093/acprof:oso/9780195178043.001.0001 · Cited by 1,026 · see citing works
Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point
Johnson, A., & Redish, A. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3761-07.2007 · Cited by 1,003 · see citing works
The Hippocampo-Neocortical Dialogue
Buzsáki, G. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.81 · Cited by 938 · see citing works
Hippocampal sharp waves: Their origin and significance
Buzsáki, G. (1986) · Brain Research · doi:10.1016/0006-8993(86)91483-6 · Cited by 925 · see citing works
Remembering episodes: a selective role for the hippocampus during retrieval
Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y., & Engel, S. A. (2000) · Nature Neuroscience · doi:10.1038/80671 · Cited by 906 · see citing works
Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.013 · Cited by 872 · see citing works
Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat
Ego‐Stengel, V., & Wilson, M. A. (2010) · Hippocampus · doi:10.1002/hipo.20707 · Cited by 842 · see citing works
Hippocampal replay of extended experience
Davidson, T. J., Kloosterman, F., & Wilson, M. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.027 · Cited by 806 · cited 1× · see citing works
“Examination of hippocampal activity during exploration of a larger environment revealed that both forward and reverse replay events can span long distances and extend across multiple SWR”
BackgroundNetwork reset: a simplified overarching theory of locus coeruleus noradrenaline function
Bouret, S., & Sara, S. J. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.09.002 · Cited by 806 · see citing works
Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1
Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M., & Moser, E. I. (2004) · Science · doi:10.1126/science.1100265 · Cited by 774 · see citing works
Awake replay of remote experiences in the hippocampus
Karlsson, M. P., & Frank, L. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2344 · Cited by 769 · cited 1× · see citing works
“In contrast, as we argue below, awake replay is consistent with the patterns of activity necessary to support a hippocampal retrieval mechanism, indicating that hippocampal replay during the awake state could be a common neural mechanism for both consolidation and retrieva”
ResultSelf-citationThe reorganization and reactivation of hippocampal maps predict spatial memory performance
Dupret, D., O'Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010) · Nature Neuroscience · doi:10.1038/nn.2599 · Cited by 769 · see citing works
Replay of rule-learning related neural patterns in the prefrontal cortex during sleep
Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., & Battaglia, F. P. (2009) · Nature Neuroscience · doi:10.1038/nn.2337 · Cited by 767 · see citing works
Finite scale of spatial representation in the hippocampus
Kjelstrup, K. B., Solstad, T., Brun, V. H., Hafting, T., Leutgeb, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2008) · Science · doi:10.1126/science.1157086 · Cited by 760 · see citing works
Kudrimoti, H. S., Barnes, C. A., & McNaughton, B. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04090.1999 · Cited by 753 · see citing works
Hippocampal replay is not a simple function of experience
Gupta, A. S., van der Meer, M. A. A., Touretzky, D. S., & Redish, A. D. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.034 · Cited by 733 · see citing works
Molecular mechanisms of memory acquisition, consolidation and retrieval
Abel, T. G., & Lattal, K. M. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00194-x · Cited by 689 · see citing works
Chrobak, J. J., & Buzsáki, G. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-03056.1996 · Cited by 587 · see citing works
Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep
Euston, D. R., Tatsuno, M., & McNaughton, B. L. (2007) · Science · doi:10.1126/science.1148979 · Cited by 586 · see citing works
Dopamine: a potential substrate for synaptic plasticity and memory mechanisms
Jay, T. M. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00085-6 · Cited by 576 · see citing works
The Neuropsychology of Human Memory
Squire, L. R. (1982) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.05.030182.001325 · Cited by 574 · see citing works
Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty
Li, S., Cullen, W. K., Anwyl, R., & Rowan, M. J. (2003) · Nature Neuroscience · doi:10.1038/nn1049 · Cited by 568 · see citing works
Huang, Y.-Y., & Kandel, E. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2446 · Cited by 544 · see citing works
Hippocampal theta oscillations are travelling waves
Lubenov, E. V., & Siapas, A. G. (2009) · Nature · doi:10.1038/nature08010 · Cited by 543 · see citing works
Chapter 1 Chapter Neurons, numbers and the hippocampal network
Amaral, D. G., Ishizuka, N., & Claiborne, B. J. (1990) · Progress in brain research · doi:10.1016/s0079-6123(08)61237-6 · Cited by 523 · see citing works
D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949
Morris, R. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00182-3 · Cited by 520 · see citing works
Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events
Csicsvari, J. L., Hirase, H., Mamiya, A., & Buzsáki, G. (2000) · Neuron · doi:10.1016/s0896-6273(00)00135-5 · Cited by 503 · see citing works
Recollection-like memory retrieval in rats is dependent on the hippocampus
Fortin, N. J., Wright, S. P., & Eichenbaum, H. (2004) · Nature · doi:10.1038/nature02853 · Cited by 460 · see citing works
Play it again: reactivation of waking experience and memory
O’Neill, J., Pleydell-Bouverie, B., Dupret, D., & Csicsvari, J. L. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.006 · Cited by 448 · see citing works
Coordinated Reactivation of Distributed Memory Traces in Primate Neocortex
Hoffman, K. L., & McNaughton, B. L. (2002) · Science · doi:10.1126/science.1073538 · Cited by 420 · see citing works
Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments
Frank, L. M., Stanley, G. B., & Brown, E. N. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1958-04.2004 · Cited by 410 · see citing works
Self-citationHippocampus leads ventral striatum in replay of place-reward information
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., McNaughton, B. L., & Pennartz, C. M. A. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000173 · Cited by 400 · see citing works
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus
Singer, A. C., & Frank, L. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.016 · Cited by 385 · see citing works
Self-citationMemory trace reactivation in hippocampal and neocortical neuronal ensembles
Sutherland, G. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00079-9 · Cited by 384 · see citing works
Ylinen, A., Soltész, I., Bragin, A., Penttonen, M., Attila Gabor, S. I. K., & Buzsáki, G. (1995) · Hippocampus · doi:10.1002/hipo.450050110 · Cited by 383 · see citing works
Configural association theory and the hippocampal formation: An appraisal and reconfiguration
Rudy, J. W., & Sutherland, R. J. (1995) · Hippocampus · doi:10.1002/hipo.450050502 · Cited by 379 · see citing works
Chrobak, J. J., & Buzsáki, G. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-10-06160.1994 · Cited by 360 · see citing works
tFast Network Oscillations in the Hippocampal CA1 Region of the Behaving Rat
Csicsvari, T., Hirase, H., Czurkó, A., Mamiya, A., & Buzsáki, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-j0001.1999 · Cited by 353 · see citing works
Frey, U., Schroeder, H., & Matthies, H. (1990) · Brain Research · doi:10.1016/0006-8993(90)91578-5 · Cited by 333 · see citing works
Reactivation of experience-dependent cell assembly patterns in the hippocampus
O'Neill, J., Senior, T. J., Allen, K., Huxter, J. R., & Csicsvari, J. (2008) · Nature Neuroscience · doi:10.1038/nn2037 · Cited by 318 · see citing works
State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep
Wierzynski, C. M., Lubenov, E. V., Gu, M., & Siapas, A. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.011 · Cited by 289 · see citing works
New Experiences Enhance Coordinated Neural Activity in the Hippocampus
Cheng, S., & Frank, L. M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.035 · Cited by 286 · see citing works
Self-citationPennartz, C. M. A., Lee, E., Verheul, J., Lipa, P., Barnes, C. A., & McNaughton, B. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0575-04.2004 · Cited by 282 · see citing works
Hippocampal CA3 Output Is Crucial for Ripple-Associated Reactivation and Consolidation of Memory
Nakashiba, T., Buhl, D. L., McHugh, T. J., & Tonegawa, S. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.013 · Cited by 281 · see citing works
O'Neill, J., Senior, T., & Csicsvari, J. (2006) · Neuron · doi:10.1016/j.neuron.2005.10.037 · Cited by 281 · see citing works
Giovannini, M. G., Rakovska, A., Benton, R. S., Pazzagli, M., Bianchi, L., & Pepeu, G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00266-4 · Cited by 267 · see citing works
McClelland, J. L., & Goddard, N. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 262 · see citing works
Network Dynamics Underlying the Formation of Sparse, Informative Representations in the Hippocampus
Karlsson, M. P., & Frank, L. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4261-08.2008 · Cited by 217 · see citing works
Self-citationvan der Meer, M. A. A., Johnson, A. C., Schmitzer-Torbert, N. C., & Redish, A. D. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.023 · Cited by 210 · see citing works
Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks
Sutherland, R. J., Weisend, M. P., Mumby, D. G., Astur, R. S., Hanlon, F. M., Koerner, A., Thomas, M. J., Wu, Y., Moses, S. N., Cole, C., et al. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 190 · see citing works
Slow-wave sleep takes the leading role in memory reorganization
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762-c2 · Cited by 177 · see citing works
Csicsvari, J. L., O'Neill, J., Allen, K. L., & Senior, T. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05684.x · Cited by 145 · see citing works
Jackson, J. C., Johnson, A. C., & Redish, A. D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4118-06.2006 · Cited by 128 · see citing works
The hippocampal complex and long-term memory revisited
Nadel, L., & Moscovitch, M. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01664-8 · Cited by 125 · see citing works
Dissociating the past from the present in the activity of place cells
de Hoz, L., & Wood, E. R. (2006) · Hippocampus · doi:10.1002/hipo.20207 · Cited by 26 · see citing works
Episodic memory, semantic memory, and amnesia
Squire, L. R., & Zola, S. M. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:3
Flagged first, then by citations
Research works printed but not linked: 1
- [19]Squire LR Clark RE Knowlton BJ Retrograde amnesia Hippocampus 2001 11 50 55 11261772
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“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 key problems arising…”
BackgroundHippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Mind-wandering as spontaneous thought: a dynamic framework
Christoff, K., Irving, Z. C., Fox, K. C. R., Spreng, R. N., & Andrews-Hanna, J. R. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.113 · Cited by 1,376 · see citing works
Gamma frequency entrainment attenuates amyloid load and modifies microglia
Iaccarino, H. F., Singer, A. C., Martorell, A. J., Rudenko, A., Gao, F., Gillingham, T. Z., Mathys, H., Seo, J., Kritskiy, O., Abdurrob, F., et al. (2016) · Nature · doi:10.1038/nature20587 · Cited by 1,328 · see citing works
Memory engrams: Recalling the past and imagining the future
Josselyn, S. A., & Tonegawa, S. (2020) · Science · doi:10.1126/science.aaw4325 · Cited by 1,087 · see citing works
Awake hippocampal sharp-wave ripples support spatial memory
Jadhav, S. P., Kemere, C., German, P. W., & Frank, L. M. (2012) · Science · doi:10.1126/science.1217230 · Cited by 924 · see citing works
Self-citationTime cells in the hippocampus: a new dimension for mapping memories
Eichenbaum, H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3827 · Cited by 843 · see citing works
The Consolidation and Transformation of Memory
Dudai, Y., Karni, A., & Born, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.004 · Cited by 741 · see citing works
What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated
Kumaran, D., Hassabis, D., & McClelland, J. L. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.05.004 · Cited by 736 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Rhythms of the hippocampal network
Colgin, L. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.21 · Cited by 654 · see citing works
Buzsáki, G., & Watson, B. O. (2012) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2012.14.4/gbuzsaki · Cited by 579 · see citing works
Reinforcement learning and episodic memory in humans and animals: an integrative framework
Gershman, S. J., & Daw, N. D. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033625 · Cited by 446 · see citing works
The hippocampal sharp wave-ripple in memory retrieval for immediate use and consolidation
Joo, H. R., & Frank, L. M. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0077-1 · Cited by 430 · see citing works
Self-citationBrain-inspired replay for continual learning with artificial neural networks
van de Ven, G. M., Siegelmann, H. T., & Tolias, A. S. (2020) · Nature Communications · doi:10.1038/s41467-020-17866-2 · Cited by 474 · see citing works
Disruption of oligodendrogenesis impairs memory consolidation in adult mice
Steadman, P. E., Xia, F., Ahmed, M., Mocle, A. J., Penning, A. R. A., Geraghty, A. C., Steenland, H. W., Monje, M., Josselyn, S. A., & Frankland, P. W. (2020) · Neuron · doi:10.1016/j.neuron.2019.10.013 · Cited by 426 · see citing works
If deep learning is the answer, what is the question?
Saxe, A., Nelli, S., & Summerfield, C. (2021) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-00395-8 · Cited by 397 · see citing works
Foster, D. J. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031538 · Cited by 375 · see citing works
Hippocampal theta sequences reflect current goals
Wikenheiser, A. M., & Redish, A. D. (2015) · Nature Neuroscience · doi:10.1038/nn.3909 · Cited by 367 · see citing works
REM sleep reorganizes hippocampal excitability
Grosmark, A. D., Mizuseki, K., Pastalkova, E., Diba, K., & Buzsáki, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.015 · Cited by 344 · see citing works
Sleep—A brain-state serving systems memory consolidation
Brodt, S., Inostroza, M., Niethard, N., & Born, J. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.005 · Cited by 343 · see citing works
Reverse replay of hippocampal place cells is uniquely modulated by changing reward
Ambrose, R. E., Pfeiffer, B. E., & Foster, D. J. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.047 · Cited by 292 · see citing works
Distinct hippocampal time cell sequences represent odor memories in immobilized rats
MacDonald, C. J., Carrow, S., Place, R., & Eichenbaum, H. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1537-13.2013 · Cited by 312 · see citing works
Sequential replay of nonspatial task states in the human hippocampus
Schuck, N. W., & Niv, Y. (2019) · Science · doi:10.1126/science.aaw5181 · Cited by 304 · see citing works
Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory
Vaz, A. P., Inati, S. K., Brunel, N., & Zaghloul, K. A. (2019) · Science · doi:10.1126/science.aau8956 · Cited by 267 · see citing works
Competing Roles of Slow Oscillations and Delta Waves in Memory Consolidation versus Forgetting
Kim, J., Gulati, T., & Ganguly, K. (2019) · Cell · doi:10.1016/j.cell.2019.08.040 · Cited by 254 · see citing works
Ben-Yakov, A., & Dudai, Y. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0702-11.2011 · Cited by 238 · see citing works
Hippocampal sharp-wave ripples linked to visual episodic recollection in humans
Norman, Y., Yeagle, E. M., Khuvis, S., Harel, M., Mehta, A. D., & Malach, R. (2019) · Science · doi:10.1126/science.aax1030 · Cited by 270 · see citing works
Functional and structural underpinnings of neuronal assembly formation in learning
Holtmaat, A., & Caroni, P. (2016) · Nature Neuroscience · doi:10.1038/nn.4418 · Cited by 239 · see citing works
Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory
Tambini, A., & Davachi, L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308499110 · Cited by 230 · see citing works
Awake reactivation predicts memory in humans
Staresina, B. P., Alink, A., Kriegeskorte, N., & Henson, R. N. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311989110 · Cited by 219 · see citing works
Internally generated sequences in learning and executing goal-directed behavior
Pezzulo, G., van der Meer, M. A. A., Lansink, C. S., & Pennartz, C. M. A. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.06.011 · Cited by 217 · see citing works
A neural-level model of spatial memory and imagery
Bicanski, A., & Burgess, N. (2018) · eLife · doi:10.7554/elife.33752 · Cited by 230 · see citing works
How memory replay in sleep boosts creative problem-solving
Lewis, P. A., Knoblich, G., & Poe, G. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.03.009 · Cited by 210 · see citing works
Shin, J. D., Tang, W., & Jadhav, S. P. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.012 · Cited by 199 · see citing works
Self-citationHippocampal awake replay in fear memory retrieval
Wu, C.-T., Haggerty, D., Kemere, C., & Ji, D. (2017) · Nature Neuroscience · doi:10.1038/nn.4507 · Cited by 210 · see citing works
Post-learning hippocampal dynamics promote preferential retention of rewarding events
Gruber, M. J., Ritchey, M., Wang, S.-F., Doss, M. K., & Ranganath, C. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.017 · Cited by 212 · see citing works
Hippocampal Replay Captures the Unique Topological Structure of a Novel Environment
Wu, X., & Foster, D. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3414-13.2014 · Cited by 201 · see citing works
Memory trace replay: The shaping of memory consolidation by neuromodulation
Atherton, L. A., Dupret, D., & Mellor, J. R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.07.004 · Cited by 180 · see citing works
Automated long-term recording and analysis of neural activity in behaving animals
Dhawale, A. K., Poddar, R., Wolff, S. B., Normand, V. A., Kopelowitz, E., & Ölveczky, B. P. (2017) · eLife · doi:10.7554/elife.27702 · Cited by 159 · see citing works
Hippocampal-prefrontal reactivation during learning is stronger in awake compared with sleep states
Tang, W., Shin, J. D., Frank, L. M., & Jadhav, S. P. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2291-17.2017 · Cited by 160 · see citing works
Self-citationHippocampal immediate poststimulus activity in the encoding of consecutive naturalistic episodes
Ben-Yakov, A., Eshel, N., & Dudai, Y. (2013) · Journal of Experimental Psychology: General · doi:10.1037/a0033558 · Cited by 153 · see citing works
Linde-Domingo, J., Treder, M. S., Kerrén, C., & Wimber, M. (2019) · Nature Communications · doi:10.1038/s41467-018-08080-2 · Cited by 152 · see citing works
Hippocampal sharp-wave ripples in waking and sleeping states
Roumis, D. K., & Frank, L. M. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.05.001 · Cited by 155 · see citing works
Self-citationPezzulo, G., Rigoli, F., & Chersi, F. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00092 · Cited by 163 · see citing works
PLD3 affects axonal spheroids and network defects in Alzheimer’s disease
Yuan, P., Zhang, M., Tong, L., Morse, T. M., McDougal, R. A., Ding, H., Chan, D., Cai, Y., & Grutzendler, J. (2022) · Nature · doi:10.1038/s41586-022-05491-6 · Cited by 155 · see citing works
Memory consolidation as an adaptive process
Cowan, E. T., Schapiro, A. C., Dunsmoor, J. E., & Murty, V. P. (2021) · Psychonomic Bulletin & Review · doi:10.3758/s13423-021-01978-x · Cited by 133 · see citing works
The why, what, where, when and how of goal-directed choice: neuronal and computational principles
Verschure, P. F. M. J., Pennartz, C. M. A., & Pezzulo, G. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0483 · Cited by 131 · see citing works
“In addition to storing information, the hippocampus is able to retrieve previously stored information and to self-generate internal sequences of cell activity that are subsequently used to map novel environments or situations [82–84].”
Manipulating a “Cocaine Engram” in Mice
Hsiang, H.-L. (., Epp, J. R., van den Oever, M. C., Yan, C., Rashid, A. J., Insel, N., Ye, L., Niibori, Y., Deisseroth, K., Frankland, P. W., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3327-14.2014 · Cited by 131 · see citing works
Respiration modulates olfactory memory consolidation in humans.
Arshamian, A., Iravani, B., Majid, A., & Lundström, J. N. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.3360-17.2018 · Cited by 115 · see citing works
Coherent phasic excitation during hippocampal ripples
Maier, N., Tejero-Cantero, Á., Dorrn, A. L., Winterer, J., Beed, P. S., Morris, G., Kempter, R., Poulet, J. F. A., Leibold, C., & Schmitz, D. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.016 · Cited by 126 · see citing works
Sleep and the functional connectome
Picchioni, D., Duyn, J. H., & Horovitz, S. G. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.067 · Cited by 115 · see citing works
Reward revaluation biases hippocampal replay content away from the preferred outcome
Carey, A. A., Tanaka, Y., & van der Meer, M. A. A. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0464-6 · Cited by 106 · see citing works
Organizing memories for generalization in complementary learning systems
Sun, W., Advani, M., Spruston, N., Saxe, A., & Fitzgerald, J. E. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01382-9 · Cited by 103 · see citing works
Replay of Episodic Memories in the Rat
Panoz-Brown, D., Iyer, V., Carey, L. M., Sluka, C. M., Rajic, G., Kestenman, J., Gentry, M., Brotheridge, S., Somekh, I., Corbin, H. E., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.04.006 · Cited by 101 · see citing works
Coordinated emergence of hippocampal replay and theta sequences during post-natal development
Muessig, L., Lasek, M., Varsavsky, I., Cacucci, F., & Wills, T. J. (2019) · Current Biology · doi:10.1016/j.cub.2019.01.005 · Cited by 91 · see citing works
Hippocampal replay of experience at real-world speeds
Denovellis, E. L., Gillespie, A. K., Coulter, M. E., Sosa, M., Chung, J. E., Eden, U. T., & Frank, L. M. (2021) · eLife · doi:10.7554/elife.64505 · Cited by 89 · see citing works
Self-citationNeuronal Responses to Conspecifics in the Ventral CA1
Rao, R. P., von Heimendahl, M., Bahr, V., & Brecht, M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.081 · Cited by 85 · see citing works
Spontaneous thought as an unconstrained memory process
Mildner, J. N., & Tamir, D. I. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.09.001 · Cited by 83 · see citing works
The sleep benefit in episodic memory: An integrative review and a meta-analysis.
Berres, S., & Erdfelder, E. (2021) · Psychological Bulletin · doi:10.1037/bul0000350 · Cited by 74 · see citing works
Findings of the BabyLM Challenge: Sample-Efficient Pretraining on Developmentally Plausible Corpora
Warstadt, A., Mueller, A., Choshen, L., Wilcox, E., Zhuang, C., Ciro, J., Mosquera, R., Paranjabe, B., Williams, A., Linzen, T., et al. (2023) · Proceedings of the BabyLM Challenge at the 27th Conference on Computational Natural Language Learning · doi:10.18653/v1/2023.conll-babylm.1 · Cited by 74 · see citing works
“While it is unlikely that humans process data iteratively in a manner similar to epoch-based training, there is evidence that humans do repeat some of the information they process (e.g., in memory replay, Carr et al., 2011).”
Brain mechanisms underlying the subjective experience of remembering
Simons, J. S., Ritchey, M., & Fernyhough, C. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-030221-025439 · Cited by 70 · see citing works
Learned motor patterns are replayed in human motor cortex during sleep
Rubin, D. B., Hosman, T., Kelemen, J. N., Kapitonava, A., Willett, F. R., Coughlin, B. F., Halgren, E., Kimchi, E. Y., Williams, Z. M., Simeral, J. D., et al. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.2074-21.2022 · Cited by 57 · see citing works
Brain State Dependence of Hippocampal Subthreshold Activity in Awake Mice
Hulse, B. K., Lubenov, E. V., & Siapas, A. G. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.11.084 · Cited by 40 · see citing works
A bird-brain view of episodic memory
Rattenborg, N. C., & Martinez-Gonzalez, D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.030 · Cited by 45 · see citing works
Replay of incidentally encoded episodic memories in the rat
Sheridan, C. L., Lang, S., Knappenberger, M., Albers, C., Loper, R., Tillett, B., Sanchez, J., Wilcox, A., Harrison, T., Panoz-Brown, D., et al. (2024) · Current Biology · doi:10.1016/j.cub.2023.12.043 · Cited by 40 · see citing works
Kuriyama, K., Honma, M., Yoshiike, T., & Kim, Y. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.045 · Cited by 36 · see citing works
Watanabe, T., Kimura, H. M., Hirose, S., Wada, H., Imai, Y., Machida, T., Shirouzu, I., Miyashita, Y., & Konishi, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5553-11.2012 · Cited by 28 · see citing works
Memory leaks: information shared across memory systems
Robertson, E. M. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.03.010 · Cited by 20 · see citing works
Self-Net: Lifelong Learning via Continual Self-Modeling
Mandivarapu, J. K., Camp, B., & Estrada, R. (2020) · Frontiers in Artificial Intelligence · doi:10.3389/frai.2020.00019 · Cited by 14 · see citing works
Time-dependent consolidation mechanisms of durable memory in spaced learning
Yang, Y., Huang, Z., Yang, Y., Fan, M., & Yin, D. (2025) · Communications Biology · doi:10.1038/s42003-025-07964-6 · Cited by 10 · see citing works
Making Memories: Why Time Matters
Kelley, P., Evans, M. D. R., & Kelley, J. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00400 · Cited by 10 · see citing works
Bigger is not always better: The importance of human-scale language modeling for psycholinguistics
Wilcox, E. G., Hu, M. Y., Mueller, A., Warstadt, A., Choshen, L., Zhuang, C., Williams, A., Cotterell, R., & Linzen, T. (2025) · Journal of Memory and Language · doi:10.1016/j.jml.2025.104650 · Cited by 9 · see citing works
- Authors
- Carr, M. F., Jadhav, S. P., & Frank, L. M.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Frank, Loren M
- Venue
- Nature Neuroscience
- Published
- 2011-01-26
- Volume
- 14
- Issue
- 2
- Pages
- 147-153
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3215304
- OpenAlex
- W1974367810
- Cited by
- 958
- References
- 82
- Citations by year
- 2026: 52 · 2025: 93 · 2024: 79 · 2023: 61 · 2022: 75 · 2021: 55 · 2020: 60 · 2019: 79 · 2018: 85 · 2017: 75 · 2016: 59 · 2015: 46 · 2014: 53 · 2013: 36 · 2012: 33
- FWCI
- 3.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH080283)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- hippocampal replay, awake state, memory consolidation, memory retrieval, place cells, hippocampus, spatial memory, event memory, sleep-dependent memory, sensory input, neural reactivation
- MeSH terms
- Hippocampus, Humans, Memory, Neurons, Sleep, Wakefulness
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