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Hippocampal Replay of Extended Experience
Open accessAbstract
During pauses in exploration, ensembles of place cells in the rat hippocampus re-express firing sequences corresponding to recent spatial experience. Such "replay" co-occurs with ripple events: short-lasting (approximately 50-120 ms), high-frequency (approximately 200 Hz) oscillations that are associated with increased hippocampal-cortical communication. In previous studies, rats exploring small environments showed replay anchored to the rat's current location and compressed in time into a single ripple event. Here, we show, using a neural decoding approach, that firing sequences corresponding to long runs through a large environment are replayed with high fidelity and that such replay can begin at remote locations on the track. Extended replay proceeds at a characteristic virtual speed of approximately 8 m/s and remains coherent across trains of ripple events. These results suggest that extended replay is composed of chains of shorter subsequences, which may reflect a strategy for the storage and flexible expression of memories of prolonged experience.
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“The reactivation of task-relevant regions was found to be particular prominent during sleep oscillatory events linked to memory consolidation, such as spindles and SOs.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [108]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“both sleep and wake replay can represent knowledge about an environment and also share anticipatory features, such that they can e.g., include offline ''pre-activations'' of trajectories entailing visible but yet unexplored paths and locations.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [148]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“Spindle activity is increased over cortical regions involved in prior learning and, moreover, positively correlates with post sleep retrieval performance 180,181 and appears to accompany memory reactivations during sleep.108,114”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [108]
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“Reactivations of hippocampal cell firing patterns occur also during waking when the animal rests after task performance or during brief pauses of active behavior like explo-ration or running in a maze (191, 268, 556, 673, 870; see Ref. 175 for a review).”
From About Sleep's Role in Memory (2013) · cites this paper as [268]
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“In larger experimental environments, both forward and reverse replay can occur over multiple SW-R events thereby covering longer distances (268).”
From About Sleep's Role in Memory (2013) · cites this paper as [268]
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“Sequences during awake LIA can occur in the opposite order of experience (backward sequences; [ 29 , 32 , 75 , 76 ]).”
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“Remarkably, place cells spike not only during active navigation but also during quiescent wake states [5, 6] and even during sleep [7–9].”
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InfluentialDisruption of theta-timescale spiking impairs learning but spares hippocampal replayPreprint
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“This is the case for example when decoding motor commands for prosthetics [3] or when decoding the ’position’ of an animal from place cell activities during memory recall [6].”
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Ormond, J., Serka, S. A., & Johansen, J. P. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/682831 · Cited by 1
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“Accordingly, ripples are considered to play a crucial role in memory processes and reorganization of memory engrams (Buzsáki, 2015; Davidson et al., 2009; Diba and Buzsáki, 2007; Dragoi and Tonegawa, 2011; Foster and Wilson, 2006; Girardeau et al., 2009; Girardeau and Zugaro, 2011; Pfeiffer and Foster, 2015; Takahashi…”
BackgroundWatanabe, Y., Ikegaya, Y., & Yanagisawa, T. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.28.538785 · Cited by 1
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BackgroundMethodSelf-citationStochastic characterization of navigation strategies in an automated variant of the Barnes mazePreprint
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“To examine coding of relative position at the population level, we used a Bayesian decoder (Skaggs et al., 1996; Davidson et al., 2009) to predict the animal’s position from the activity of simultaneously recorded PFC neurons.”
MethodChoi, J., Carmichael, J. E., Williams, S., & Etter, G. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.05.611474 · Cited by 1
“…populations with complementary methods spanning progressively stronger assumptions about temporal order, co-activity 25,38,39 , Bayesian decoding 40,41 , and sequence factorization 26 , and by cross-validating against conservative surrogates, we recovered structure that any single approach could…”
Adam, C. D., Mirzakhalili, E., Gagnon, K. G., Cottone, C., Arena, J. D., Ulyanova, A. V., Johnson, V. E., & Wolf, J. A. (2024) · eLife · doi:10.7554/elife.100642 · Cited by 1
“…higher frequency sharp-wave ripples (SWRs) are known to support working memory processes and memory consolidation ( Buzsáki, 1986 ; Buzsáki, 2015 ; Carr et al., 2011 ; Davidson et al., 2009 ; Wilson and McNaughton, 1994 ), however, the effects of TBI on these processes have not been investigated.”
Adam, C. D., Mirzakhalili, E., Gagnon, K. G., Cottone, C., Arena, J. D., Ulyanova, A. V., Johnson, V. E., & Wolf, J. A. (2024) · eLife · doi:10.7554/elife.100642.1 · Cited by 1
Shimbo, A., Sekine, Y., Kashiwagi, S., & Fujisawa, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.10.622881 · Cited by 1
Modeling flexible behavior with remapping-based hippocampal sequence learningPreprint
Ito, Y., & Toyoizumi, T. (2025) · eLife · doi:10.7554/elife.106506 · Cited by 2
Spontaneous reinstatement of episodic memories in the developing human brainPreprint
Yates, T. S., Callaghan, B. L., Silvers, J. A., VanTieghem, M., Choy, T., O’Sullivan, K., Davachi, L., & Tottenham, N. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.15.676365 · Cited by 1
“…learned spatial patterns in rodents during both sleep and wake states (Skaggs & McNaughton, 1996; Wilson & McNaughton, 1994; Foster & Wilson, 2006; Davidson et al., 2009; Carr et al., 2011), functional neuroimaging in human adults has shown memory reinstatement during awake rest in the…”
A Spiking Neural Model of Episodic Memory Encoding and Replay in Hippocampus
Trujillo, O. (2014) · UWSpace (University of Waterloo) · Cited by 1
Spontaneous emergence and evolution of neuronal sequences in recurrent networksPreprint
Shao, S., Riquelme, J. L., & Gjorgjieva, J. (2026) · eLife · doi:10.7554/elife.110718.1 · Cited by 2
Spontaneous emergence and evolution of neuronal sequences in recurrent networksPreprint
Shao, S., Riquelme, J. L., & Gjorgjieva, J. (2026) · eLife · doi:10.7554/elife.110718 · Cited by 3
The temporal and bilateral structure of hippocampal replay
Layton, S. P. (2013) · DSpace@MIT (Massachusetts Institute of Technology)
Signal-To-Noise-Optimal scaling of heterogenous population codes
Leibold, C. (2013) · Network Computation in Neural Systems · doi:10.3109/0954898x.2013.822117
“Examples for such population codes are the place map of the hippocampus (O’Keefe and Dostrovsky 1971; Davidson et al. 2009), the representation of odors in the olfactory system (Laurent 2002), the orientation code in primary visual cortex (Kelly et al. 2007), and the representation of auditory…”
BackgroundHippocampal contributions to value-guided foraging
Wikenheiser, A. M. (2014) · University of Minnesota Digital Conservancy (University of Minnesota)
Demchuk, A. M. (2014) · Open ULeth Scholarship (OPUS) (University of Lethbridge)
Information-geometric method for multiple neuronal spike data analysis
Nie, Y. (2014) · Open ULeth Scholarship (OPUS) (University of Lethbridge)
Inter-regional synchronization in the hippocampal system by oscillations
Sullivan, D. W. (2013) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t33n221m
Prefrontal-thalamo-hippocampal circuit contributions to spatial working memory
Hallock, H. L. (2024) · Library, Museums and Press - UDSpace (University of Delaware) · doi:10.58088/91j6-wc29
Electrophysiological Approaches for Studying Neuronal Circuits In Vivo
Dragoi, G. (2011) · Neuromethods · doi:10.1007/7657_2011_21
Information Geometric Analysis of Neurophysiological Data
Tatsuno, M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802452-2.00002-0
Neural plasticity in decision making and memory formation
Garvert, M. M. (2016) · UCL Discovery (University College London)
Effect of cognitive state on the consolidation of basic and complex memories
Craig, M. (2016) · ERA
Pu, Y., Cornwell, B. R., Cheyne, D., & Johnson, B. W. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/252288
Prior-knowledge Effects on Associative Memory Processing
Liu, Z. X. (2015) · TSpace (University of Toronto)
Metadata
- Authors
- Davidson, T. J., Kloosterman, F., & Wilson, M. A.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Kloosterman, Fabian
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2009-08
- Volume
- 63
- Issue
- 4
- Pages
- 497-507
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4364032
- OpenAlex
- W2079161053
- Cited by
- 806
- References
- 53
- Citations by year
- 2026: 41 · 2025: 54 · 2024: 68 · 2023: 57 · 2022: 56 · 2021: 65 · 2020: 49 · 2019: 72 · 2018: 42 · 2017: 41 · 2016: 49 · 2015: 42 · 2014: 57 · 2013: 40 · 2012: 26
- FWCI
- 11.45
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1477 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Lirias (KU Leuven) (submittedVersion)
- Funders
- National Institutes of Health (MH061976)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampal replay, place cells, spatial memory, neural decoding, memory storage
- MeSH terms
- Animals, Exploratory Behavior, Hippocampus, Learning, Male, Spatial Behavior, Time Factors, Rats, Long-Evans, Rats
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