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The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats
Abstract
The mechanisms underlying off-line consolidation of memory during sleep are elusive. Learning of hippocampus-dependent tasks increases neocortical slow oscillation synchrony, and thalamocortical spindle and hippocampal ripple activity during subsequent non-rapid eye movement sleep. Slow oscillations representing an oscillation between global neocortical states of increased (up-state) and decreased (down-state) neuronal firing temporally group thalamic spindle and hippocampal ripple activity, which both occur preferentially during slow oscillation up-states. Here we examined whether slow oscillations also group learning-induced increases in spindle and ripple activity, thereby providing time-frames of facilitated hippocampus-to-neocortical information transfer underlying the conversion of temporary into long-term memories. Learning (word-pairs in humans, odor-reward associations in rats) increased slow oscillation up-states and, in humans, shaped the timing of down-states. Slow oscillations grouped spindle and rat ripple activity into up-states under basal conditions. Prior learning produced in humans an increase in spindle activity focused on slow oscillation up-states. In rats, learning induced a distinct increase in spindle and ripple activity that was not synchronized to up-states. Event-correlation histograms indicated an increase in spindle activity with the occurrence of ripples. This increase was prolonged after learning, suggesting a direct temporal tuning between rip…
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In the citing paper
“In humans, intense learning of declarative memories (word pairs) enhanced amplitudes of the slow oscillation up-states as well as coherence in the SWA frequency band during succeeding SWS (829, 831).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“Also, slopes of the down-to-up state of the slow oscillations were steeper after learning.”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“At the neocortical level, the slow oscillation in terms of EEG rhythms strongly modulates the amplitude of faster beta and gamma frequencies which is reduced to a minimum during the hyperpolarizing down-phase of the slow oscillation (224,240,828,829).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“In humans, intense learning of vocabulary did not only increase the slope of the down-to-up state transition of the slow oscillation during succeeding non-REM sleep, but concurrently enhanced fast spindle activity, with this increase concentrating on the up-states of the slow oscillation, whereas no changes were observed in hyperpolarizing down-states (826, 829).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“Generation of spindles in the thalamus and generation of SW-Rs in the hippocampus are distinctly suppressed during the down-phase of the slow oscillation, and this is followed by a rebound in spindle and SW-R activity during the succeeding depolarizing up-state (66, 215, 597, 829 -832, 925, 1088).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
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Metadata
- Authors
- Mölle, M., Eschenko, O., Gais, S., Sara, S. J., & Born, J.
- Affiliations
- University of Lübeck (DE)
- Centre National de la Recherche Scientifique (FR)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2009-03
- Volume
- 29
- Issue
- 5
- Pages
- 1071-1081
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2163770201
- Cited by
- 322
- References
- 71
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 18 · 2023: 17 · 2022: 17 · 2021: 13 · 2020: 24 · 2019: 46 · 2018: 18 · 2017: 20 · 2016: 19 · 2015: 16 · 2014: 17 · 2013: 22 · 2012: 16
- FWCI
- 7.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- sleep slow oscillations, sleep spindles, hippocampal ripples, memory consolidation, hippocampus-dependent learning, word pair learning, NREM sleep
- MeSH terms
- Adult, Animals, Association Learning, Cerebral Cortex, Electroencephalography, Evoked Potentials, Female, Humans, Male, Neuropsychological Tests, Odorants, Periodicity, Reward, Sleep, Spectrum Analysis, Statistics as Topic, Rats, Sprague-Dawley, Rats, Young Adult
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