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Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Open accessAbstract
High-frequency oscillations, known as sharp-wave/ripple (SPW-R) complexes occurring in hippocampus during slow-wave sleep (SWS), have been proposed to promote synaptic plasticity necessary for memory consolidation. We recorded sleep for 3 h after rats were trained on an odor-reward association task. Learning resulted in an increased number SPW-Rs during the first hour of post-learning SWS. The magnitude of ripple events and their duration were also elevated for up to 2 h after the newly formed memory. Rats that did not learn the discrimination during the training session did not show any change in SPW-Rs. Successful retrieval from remote memory was likewise accompanied by an increase in SPW-R density and magnitude, relative to the previously recorded baseline, but the effects were much shorter lasting and did not include increases in ripple duration and amplitude. A short-lasting increase of ripple activity was also observed when rats were rewarded for performing a motor component of the task only. There were no increases in ripple activity after habituation to the experimental environment. These experiments show that the characteristics of hippocampal high-frequency oscillations during SWS are affected by prior behavioral experience. Associative learning induces robust and sustained (up to 2 h) changes in several SPW-R characteristics, while after retrieval from remote memory or performance of a well-trained procedural aspect of the task, only transient changes in ripple density were induced.
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“Also, consistent with this concept, at the level of local field potentials, slow oscillations, spindle activity and hippocampal ripple activity are increased during sleep after a learning experience (Gais, Molle, Helms, & Born 2002; Eschenko, Ramadan, Molle, Born, & Sara 2008; Mölle & Born 2009)”
From System consolidation of memory during sleep (2012) · cites this paper as Eschenko, Ramadan, Molle, Born, & Sara 2008
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“The results of the present study do lend further support to a substantial body of literature from human and animal studies suggesting the importance of off-line information processing and SWS-associated memory consolidation (Pennartz et al. 2002; Gais and Born 2004; Ribeiro and Nicolelis 2004; Stickgold 2005; Walker a…”
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Alger, S. E., Chambers, A. M., Cunningham, T. J., & Payne, J. D. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_341 · Cited by 55
The Common Effects of Sleep Deprivation on Human Long-Term Memory and Cognitive Control Processes
Kim, T., Kim, S., Kang, J., Kwon, M., & Lee, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.883848 · Cited by 56
The role of experience in prioritizing hippocampal replay
Gorriz, M. H., Takigawa, M., & Bendor, D. (2023) · Nature Communications · doi:10.1038/s41467-023-43939-z · Cited by 59
Metadata
- Authors
- Eschenko, O., Ramadan, W., Mölle, M., Born, J., & Sara, S. J.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- University of Lübeck (DE)
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2008-04
- Volume
- 15
- Issue
- 4
- Pages
- 222-228
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- PMC
- PMC2327264
- OpenAlex
- W2118168358
- Cited by
- 277
- References
- 48
- Citations by year
- 2026: 10 · 2025: 18 · 2024: 11 · 2023: 13 · 2022: 16 · 2021: 9 · 2020: 20 · 2019: 21 · 2018: 24 · 2017: 31 · 2016: 19 · 2015: 8 · 2014: 16 · 2013: 8 · 2012: 6
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, cc-by)
- Funders
- Volkswagen Foundation
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- sharp-wave ripples, slow-wave sleep, hippocampus, memory consolidation, associative learning, remote memory retrieval, high-frequency oscillations, synaptic plasticity, procedural learning
- MeSH terms
- Animals, Electroencephalography, Hippocampus, Learning, Sleep, Time Factors, Rats
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