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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.”
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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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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