Sharp wave ripples during learning stabilize the hippocampal spatial map
Open accessAbstract
Cognitive representation of the environment requires a stable hippocampal map, but the mechanisms maintaining a given map are unknown. Because sharp wave-ripples (SPW-R) orchestrate both retrospective and prospective spatial information, we hypothesized that disrupting neuronal activity during SPW-Rs affects spatial representation. Mice learned new sets of three goal locations daily in a multiwell maze. We used closed-loop SPW-R detection at goal locations to trigger optogenetic silencing of a subset of CA1 pyramidal neurons. Control place cells (nonsilenced or silenced outside SPW-Rs) largely maintained the location of their place fields after learning and showed increased spatial information content. In contrast, the place fields of SPW-R-silenced place cells remapped, and their spatial information remained unaltered. SPW-R silencing did not impact the firing rates or proportions of place cells. These results suggest that interference with SPW-R-associated activity during learning prevents stabilization and refinement of hippocampal maps.
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Wake replay is expected not to interfere with consolidation only when it is not offline but occurs briefly after encoding in the very same context as the encoded event.
“Along this line, wake replay is expected not to interfere with consolidation only when it is not ''offline'' but occurs briefly after encoding in the very same context as the encoded event.284,285,293”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [284]
The Results report that activity during awake sharp-wave ripples promotes stabilization of hippocampal place representations, and the Discussion links this effect to learning new map configurations. The paper does not establish that wake replay avoids interfering with consolidation only if it occurs briefly after encoding in the same context; its manipulation took place during learning, and it makes no such exclusive claim. (LLM, conf=0.85)
Experimental — accuracy not yet measuredDisturbing wake replay activity impairs memory formation, indicating that neuronal reactivations of newly formed representations represent a common core process for consolidation during sleep and wakefulness.
“Disturbing such wake replay activity has also been found to impair memory formation, 284,285 indicating that neuronal reactivations of newly formed representations represent a common core process for consolidation during sleep and wakefulness.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [284]
The Introduction reports that disrupting awake sharp-wave ripples can impair behavioral performance and that interfering with them during sleep can worsen memory performance. This study found that silencing neurons during awake ripples destabilized place-cell spatial representations, but its Results report no difference in measured memory performance between ripple-locked and delayed stimulation. It therefore supports a role for awake ripple activity in maintaining newly learned representations, not the stronger conclusion that this experiment demonstrated impaired memory formation or established one common consolidation process across sleep and wakefulness. (LLM, conf=0.86)
Experimental — accuracy not yet measuredReward receipt increases spike-wave ripples, which enhance place field stability and may promote learning of reward locations.
“Importantly, receipt of a reward triggers an increase in the rate of spike-wave ripples [63], which are known to enhance place field stability, and may thereby promote learning of reward locations [64].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [64]
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References 65 · Cited by 229
Research works printed but not linked: 1
- [64]Skaggs WE McNaughton BL G KM M EJ Advances in Neural Information Processing Systems Hanson SJ Cowan JD Giles CL 1993 5 1030 1037 Morgan Kaufmann
- Authors
- Roux, L., Hu, B., Eichler, R., Stark, E., & Buzsáki, G.
- Affiliations
- New York University (US)
- Radboud University Nijmegen (NL)
- Tel Aviv University (IL)
- NYU Langone Health (US)
- Corresponding author
- Buzsáki, György
- Venue
- Nature Neuroscience
- Published
- 2017-04-10
- Volume
- 20
- Issue
- 6
- Pages
- 845-853
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5446786
- OpenAlex
- W2607419807
- Semantic Scholar
- a384cd50b1cf2716e33014544d29621580769b06
- Cited by
- 229
- References
- 65
- Citations by year
- 2026: 19 · 2025: 27 · 2024: 23 · 2023: 20 · 2022: 24 · 2021: 22 · 2020: 23 · 2019: 38 · 2018: 29 · 2017: 4
- FWCI
- 14.76
- 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)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH054671, R01MH107396)
- National Institute of Neurological Disorders and Stroke (U01NS090583, K99NS094735)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- sharp-wave ripples, place cells, CA1 pyramidal neurons, optogenetic silencing, spatial learning, spatial representation, place field remapping
- MeSH terms
- Place Cells, Action Potentials, Animals, Electric Stimulation, Learning, Male, Mice, Transgenic, Neural Inhibition, Sleep, Pyramidal Cells, Maze Learning, Mice, CA1 Region, Hippocampal, Spatial Memory
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