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Hippocampal Replay Captures the Unique Topological Structure of a Novel Environment
Open accessAbstract
Hippocampal place-cell replay has been proposed as a fundamental mechanism of learning and memory, which might support navigational learning and planning. An important hypothesis of relevance to these proposed functions is that the information encoded in replay should reflect the topological structure of experienced environments; that is, which places in the environment are connected with which others. Here we report several attributes of replay observed in rats exploring a novel forked environment that support the hypothesis. First, we observed that overlapping replays depicting divergent trajectories through the fork recruited the same population of cells with the same firing rates to represent the common portion of the trajectories. Second, replay tended to be directional and to flip the represented direction at the fork. Third, replay-associated sharp-wave–ripple events in the local field potential exhibited substructure that mapped onto the maze topology. Thus, the spatial complexity of our recording environment was accurately captured by replay: the underlying neuronal activities reflected the bifurcating shape, and both directionality and associated ripple structure reflected the segmentation of the maze. Finally, we observed that replays occurred rapidly after small numbers of experiences. Our results suggest that hippocampal replay captures learned information about environmental topology to support a role in navigation.
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“as does repeated replay or rehearsal of assemblies that encode recent experiences108,109.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [109]
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Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322
Cognitive maps in rats and men
Tolman, E. C. (1948) · Psychological Review · doi:10.1037/h0061626 · Cited by 6,641
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794
Gallistel, C. R. (1990) · Cited by 2,571
A framework for mesencephalic dopamine systems based on predictive Hebbian learning
Montague, P., Dayan, P., & Sejnowski, T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01936.1996 · Cited by 2,066
Remembrance of places passed: Spatial memory in rats.
Olton, D. S., & Samuelson, R. J. (1976) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.2.2.97 · Cited by 1,993
The cognitive neuroscience of constructive memory: remembering the past and imagining the future
Schacter, D. L., & Addis, D. R. (2007) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2087 · Cited by 1,836
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
Self-citationTwo-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
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669
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
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
Hippocampal place-cell sequences depict future paths to remembered goals
Pfeiffer, B. E., & Foster, D. J. (2013) · Nature · doi:10.1038/nature12112 · Cited by 1,216
Self-citationForward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148
Requirement for Hippocampal CA3 NMDA Receptors in Associative Memory Recall
Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., Kato, A., Carr, C. A., Johnston, D., Wilson, M. A., et al. (2002) · Science · doi:10.1126/science.1071795 · Cited by 1,127
Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval
Carr, M. F., Jadhav, S. P., & Frank, L. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2732 · Cited by 958
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
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
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 13×
“Directional place fields were calculated and were used to compute joint posterior probabilities over both position and direction (Davidson et al., 2009), for the already identified replays.”
BackgroundMethodInfluentialAwake 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 4×
“It is now well established that hippocampal place cells engage in extended spiking sequences across neuronal ensembles that match sequences from previous behavioral episodes, often in a temporally condensed form during 100 –200 ms sharp-wave–ripple (SWR) events in the hippocampal local field potential (LFP; Louie and…”
BackgroundInfluentialTrajectory Encoding in the Hippocampus and Entorhinal Cortex
Frank, L. M., Brown, E. N., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00018-0 · Cited by 760
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
The global record of memory in hippocampal neuronal activity
Wood, E. R., Dudchenko, P. A., & Eichenbaum, H. (1999) · Nature · doi:10.1038/17605 · Cited by 707
Gaffan, D. (1994) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1994.6.4.305 · Cited by 484
Play it again: reactivation of waking experience and memory
O’Neill, J., Pleydell-Bouverie, B., Dupret, D., & Csicsvari, J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.006 · Cited by 480
The Role of the Hippocampus in Prediction and Imagination
Buckner, R. L. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163508 · Cited by 419
Jensen, O. B., & Lisman, J. E. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.279 · Cited by 392
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
McClelland, J. L., & Goddard, N. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 264
Morris, R. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0945 · Cited by 233
Csicsvari, J., 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 150
Sequence learning and the role of the hippocampus in rodent navigation
Foster, D. J., & Knierim, J. J. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.12.005 · Cited by 132
Self-citationMemory Capacity for Sequences in a Recurrent Network with Biological Constraints
Leibold, C., & Kempter, R. (2006) · Neural Computation · doi:10.1162/neco.2006.18.4.904 · Cited by 58
Molter, C., Sato, N., & Yamaguchi, Y. (2007) · Hippocampus · doi:10.1002/hipo.20258 · Cited by 42
Koene, R. A., & Hasselmo, M. E. (2008) · Neural Networks · doi:10.1016/j.neunet.2007.12.029 · Cited by 31
Research works printed but not linked: 1
- 10.1037//0097-7403.2.2.97 · DOI
Cited by
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Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759
The cognitive map in humans: spatial navigation and beyond
Epstein, R. A., Patai, E. Z., Julian, J. B., & Spiers, H. J. (2017) · Nature Neuroscience · doi:10.1038/nn.4656 · Cited by 921
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 759
Josselyn, S. A., Köhler, S., & Frankland, P. W. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4000 · Cited by 749
Rhythms of the hippocampal network
Colgin, L. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.21 · Cited by 654
Metadata
- Authors
- Wu, X., & Foster, D. J.
- Affiliations
- Johns Hopkins University (US)
- ORCID
- Foster, David J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-05-07
- Volume
- 34
- Issue
- 19
- Pages
- 6459-6469
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4012305
- OpenAlex
- W2002978960
- Cited by
- 201
- References
- 41
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 17 · 2023: 16 · 2022: 10 · 2021: 18 · 2020: 18 · 2019: 26 · 2018: 23 · 2017: 18 · 2016: 21 · 2015: 7 · 2014: 1
- FWCI
- 8.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alfred P. Sloan Foundation
- Whitehall Foundation
- National Institutes of Health
- National Institute of Mental Health (R01MH085823)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- hippocampal replay, place cells, maze navigation, sharp-wave ripples, local field potentials, novel environment, spatial memory
- MeSH terms
- Algorithms, Animals, Environment, Evoked Potentials, Hippocampus, Learning, Male, Neural Pathways, Neurons, Reward, Spatial Behavior, Linear Models, Maze Learning, Rats, Long-Evans, Rats, Electrophysiological Phenomena
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