The reorganization and reactivation of hippocampal maps predict spatial memory performance
Open accessAbstract
The hippocampus is an important brain circuit for spatial memory and the spatially selective spiking of hippocampal neuronal assemblies is thought to provide a mnemonic representation of space. We found that remembering newly learnt goal locations required NMDA receptor-dependent stabilization and enhanced reactivation of goal-related hippocampal assemblies. During spatial learning, place-related firing patterns in the CA1, but not CA3, region of the rat hippocampus were reorganized to represent new goal locations. Such reorganization did not occur when goals were marked by visual cues. The stabilization and successful retrieval of these newly acquired CA1 representations of behaviorally relevant places was NMDAR dependent and necessary for subsequent memory retention performance. Goal-related assembly patterns associated with sharp wave/ripple network oscillations, during both learning and subsequent rest periods, predicted memory performance. Together, these results suggest that the reorganization and reactivation of assembly firing patterns in the hippocampus represent the formation and expression of new spatial memory traces.
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Several studies identified a causal relationship between reactivation and memory consolidation.
“several studies identified a causal relationship between reactivation and memory consolidation.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [83]
The Discussion (page not provided) reports that reactivation predicts later spatial-memory performance and describes a functional link. It does not establish the claimed causal relationship: the authors say experimental evidence has been largely lacking and note that studies disrupting sharp-wave ripples could not rule out effects on consolidation through mechanisms other than reactivation. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAwake memory reactivations have been shown to enhance subsequent recall performance.
“awake memory reactivations have been shown to enhance subsequent recall performance.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [83]
The Results section (‘Reactivation of waking firing patterns during rest’; page unavailable) reports that goal-related reactivation during rest predicted subsequent spatial-memory performance, and the Discussion says reactivation predicted how well a location was remembered. The paper does not show that awake reactivations themselves enhanced recall: the reported relationship is predictive, and the rest-period events are not identified as exclusively awake. (LLM, conf=0.86)
Experimental — accuracy not yet measuredOne study reported that both the number of SW-Rs during learning a spatial task as well as during subsequent rest were predictive for later memory performance.
“One study reported that both the number of SW-Rs during learning a spatial task as well as during subsequent rest were predictive for later memory performance (335).”
From About Sleep's Role in Memory (2013) · cites this paper as [335]
The Results section on eSWR responses during learning reports that the number of goal-associated SWRs predicted memory performance in the drug-free condition. The Results section on reactivation during rest reports that the *proportion* of rest SWRs representing goal locations predicted subsequent performance, not that the total number of rest SWRs did. Page numbers are unavailable in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredSpontaneous memory reactivations during sleep correlate with later memory performance.
“and that spontaneous memory reactivations during sleep correlate with later memory performance (335, 448, 449).”
From About Sleep's Role in Memory (2013) · cites this paper as [335]
The Results section ('Reactivation of waking firing patterns during rest'; page not available) reports that goal-related reactivation during post-learning rest predicted subsequent spatial-memory performance. The Methods ('Training'; page not available) describe that rest session as 'immobility/sleep,' so the paper does not establish that the correlation was specific to reactivations during sleep. (LLM, conf=0.86)
Experimental — accuracy not yet measuredLearning reward locations reorganizes place fields so that areas near those locations become overrepresented.
“This is thought to result because the learning of reward locations results in the reorganization of place fields so that areas near those locations become overrepresented [61].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [61]
New representations formed during exploration of novel environments or learning of new goal locations are initially labile and require stabilization to persist as memories.
“However new representations, such as those formed during exploration of novel environments or learning of new goal locations, are initially labile and thus require stabilization to persist as memories4-6.”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [6]
When applied during spatial learning of new goal locations, dopaminergic photostimulation improved the later recall of neural representations of space.
“When applied during spatial learning of new goal locations, dopaminergic photostimulation improved the later recall of neural representations of space and stabilized memory performance.”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [6]
Such reactivation is thought to enable the incorporation of new memory engrams, especially those associated with novel and rewarded outcomes, into stable representations capable of informing future behavior.
“Such reactivation is thought to enable the incorporation of new memory engrams, especially those associated with novel and rewarded outcomes, into stable representations capable of informing future behavior6,11,12,18.”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [6]
Reactivation drives memory retention and manipulation of the key oscillatory mechanisms that support this process modulates memory performance.
“Indeed, reactivation drives memory retention14 and manipulation of the key oscillatory mechanisms that support this process modulates memory performance.15”
From Random auditory stimulation during sleep disturbs traveling slow waves and declarative memory (2026) · cites this paper as [14]
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“This contrasts with findings indicating that an external triggering of memory reactivations during sleep enhances memory performance the next day (295, 959, 1018) and that spontaneous memory reactivations during sleep correlate with later memory performance (335, 448, 449).”
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- Authors
- Dupret, D., O'Neill, J., Pleydell-Bouverie, B., & Csicsvari, J.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Dupret, David
- Csicsvari, Jozsef
- Venue
- Nature Neuroscience
- Published
- 2010-07-18
- Volume
- 13
- Issue
- 8
- Pages
- 995-1002
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC2923061
- OpenAlex
- W2017766656
- Cited by
- 769
- References
- 60
- Citations by year
- 2026: 46 · 2025: 69 · 2024: 77 · 2023: 65 · 2022: 64 · 2021: 61 · 2020: 51 · 2019: 68 · 2018: 51 · 2017: 40 · 2016: 38 · 2015: 29 · 2014: 32 · 2013: 30 · 2012: 22
- FWCI
- 15.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, other-oa)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampus, spatial memory, place cells, place field remapping, memory consolidation, NMDA receptor, CA1, CA3, memory reactivation
- MeSH terms
- Animals, Brain Mapping, Electrodes, Implanted, Hippocampus, Male, Memory, Space Perception, Spatial Behavior, Rats, Long-Evans, Rats
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