Reverse replay of hippocampal place cells is uniquely modulated by changing reward
Open accessAbstract
Hippocampal replays are episodes of sequential place cell activity during sharp-wave ripple oscillations (SWRs). Conflicting hypotheses implicate awake replay in learning from reward and in memory retrieval for decision making. Further, awake replays can be forward, in the same order as experienced, or reverse, in the opposite order. However, while the presence or absence of reward has been reported to modulate SWR rate, the effect of reward changes on replay, and on replay direction in particular, has not been examined. Here we report divergence in the response of forward and reverse replays to changing reward. While both classes of replays were observed at reward locations, only reverse replays increased their rate at increased reward or decreased their rate at decreased reward, while forward replays were unchanged. These data demonstrate a unique relationship between reverse replay and reward processing and point to a functional distinction between different directions of replay. VIDEO ABSTRACT.
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Decoded spatial locations during sharp-wave ripple-related reactivations clustered around the reward zone, indicating preferential reactivation of this behaviorally salient area.
“Decoded spatial locations during sharp-wave ripple–related reactivations clustered around the reward zone (Supplementary Fig. 3; see also refs. 47,48), indicating preferential reactivation of this behaviorally salient area.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [47]
The Results section reports that most replayed trajectories began at the rat’s actual location, and the paper describes forward and reverse replays occurring at reward locations. It also finds that reverse-replay rates change with reward. These passages support a relationship between replay and reward, but they do not establish that decoded spatial locations clustered around the reward zone. (LLM, conf=0.82)
Experimental — accuracy not yet measuredRepresentations of rewarded spatial locations are preferentially reactivated in both wake and sleep states, although there are also findings of a bias in the opposite direction.
“representations of rewarded spatial locations are preferentially reactivated in both wake and sleep states, 80,81,[142][143][144] although there are also findings of a bias of reactivations in the opposite direction.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [142]
The Abstract reports that awake reverse replay at reward locations increased with increased reward, while forward replay did not. The Introduction says replay also occurs during slow-wave sleep, but our copy does not establish preferential reactivation of rewarded locations during sleep. The cited paper therefore supports the awake component, not the claim across both states. (LLM, conf=0.88)
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“47,48), indicating preferential reactivation of this behaviorally salient area.”
- Authors
- Ambrose, R. E., Pfeiffer, B. E., & Foster, D. J.
- Affiliations
- Johns Hopkins University (US)
- Corresponding author
- Foster, David J.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-09
- Volume
- 91
- Issue
- 5
- Pages
- 1124-1136
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6013068
- OpenAlex
- W2507425266
- Cited by
- 292
- References
- 33
- Citations by year
- 2026: 23 · 2025: 44 · 2024: 32 · 2023: 29 · 2022: 29 · 2021: 25 · 2020: 33 · 2019: 26 · 2018: 30 · 2017: 18 · 2016: 2
- FWCI
- 16.12
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Johns Hopkins Bloomberg School of Public Health
- National Institute of Mental Health (R01MH085823, R01MH103325)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- hippocampal replay, place cells, sharp-wave ripples, reward, memory retrieval, decision-making, reward processing
- MeSH terms
- Place Cells, Animals, Hippocampus, Male, Models, Neurological, Reward, Rats
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