Dynamics of awake hippocampal-prefrontal replay for spatial learning and memory-guided decision making
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Abstract
SUMMARY Spatial learning requires remembering and choosing paths to goals. Hippocampal place cells replay spatial paths during immobility in reverse and forward order, offering a potential mechanism. However, how replay supports both goal-directed learning and memory-guided decision making is unclear. We therefore continuously tracked awake replay in the same hippocampal-prefrontal ensembles throughout learning of a spatial alternation task. We found that during pauses between behavioral trajectories, reverse and forward hippocampal replay support an internal cognitive search of available past and future possibilities, and exhibit opposing learning gradients for prediction of past and future behavioral paths, respectively. Coordinated hippocampal-prefrontal replay distinguished correct past and future paths from alternative choices, suggesting a role in recall of past paths to guide planning of future decisions for spatial working memory. Our findings reveal a learning shift from hippocampal reverse-replay-based retrospective evaluation to forward-replay-based prospective planning, with prefrontal read-out of memory-guided paths for learning and decision-making.
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Reactivation of ensemble firing patterns occurs during quiet rest and active behavior in rodents and humans, as well as during sleep.
“Reactivation of ensemble firing patterns was first identified during sleep, 79,136 but the phenomenon occurs likewise during quiet rest as well as during active behavior, in rodents 80,81,137,138 as well as in humans.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [138]
Offline replay of ensemble firing patterns in conjunction with hippocampal ripples occurs also during quiet wakefulness.
“However, the offline replay of ensemble firing patterns in conjunction with hippocampal ripples occurs also during quiet wakefulness.138,150”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [138]
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- Authors
- Shin, J. D., Tang, W., & Jadhav, S. P.
- Affiliations
- Brandeis University (US)
- Corresponding author
- Tang, Wenbo
- Jadhav, Shantanu P.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2019-12
- Volume
- 104
- Issue
- 6
- Pages
- 1110-1125.e7
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6923537
- OpenAlex
- W2982510093
- Semantic Scholar
- 8ebb0bde31a27c8b9dcb6d2f6ceb5affb2cff1dc
- Cited by
- 199
- References
- 100
- Citations by year
- 2026: 25 · 2025: 47 · 2024: 22 · 2023: 25 · 2022: 23 · 2021: 32 · 2020: 23 · 2019: 2
- FWCI
- 11.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Whitehall Foundation
- Alfred P. Sloan Foundation
- National Institutes of Health
- 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, spatial learning, memory-guided decision-making, spatial working memory, place cells, prospective planning, retrospective evaluation, cognitive search, trajectory prediction
- MeSH terms
- Animals, Decision Making, Hippocampus, Male, Memory, Short-Term, Wakefulness, Prefrontal Cortex, Rats, Long-Evans, Rats, Spatial Learning
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