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 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.
“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]
Slopes of the down-to-up state of the slow oscillations were steeper after learning.
“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]
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.
“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 humans, intense learning of vocabulary increased the slope of the down-to-up state transition of the slow oscillation during succeeding non-REM sleep, and 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.
“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]
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, followed by a rebound in spindle and SW-R activity during the succeeding depolarizing up-state.
“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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Generalization of word meanings during infant sleep
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Napping to renew learning capacity: enhanced encoding after stimulation of sleep slow oscillations
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Self-citationInvolvement of spindles in memory consolidation is slow wave sleep-specific
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“Importantly, slow oscillations have a naturally occurring grouping influence on spindles (Mölle et al. 2002; Clemens et al. 2007), and such focusing of spindle rhythms into the active slow oscillation up-state increases after a learning episode (Mölle et al. 2009).”
BackgroundSleep-dependent memory consolidation – What can be learnt from children?
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The role of inhibitory circuits in hippocampal memory processing
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NREM Sleep Oscillations and Brain Plasticity in Aging
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Primed to Sleep: The Dynamics of Synaptic Plasticity Across Brain States
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Sleep spindles preferentially consolidate weakly encoded memories
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Slow Oscillations during Sleep Coordinate Interregional Communication in Cortical Networks
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“Furthermore, an increase in spindle density or amplitude is observed in humans (for review, see Fogel and Smith, 2011) and rodents (Schiffelholz and Aldenhoff, 2002; Eschenko et al., 2006; Mölle et al., 2009) after learning tasks.”
Thalamic reticular control of local sleep in mouse sensory cortex
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A mechanism for learning with sleep spindles
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Sleep stage II contributes to the consolidation of declarative memories
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The sleeping infant brain anticipates development
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Self-citationWakefulness (Not Sleep) Promotes Generalization of Word Learning in 2.5-Year-Old Children
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Nocturnal Mnemonics: Sleep and Hippocampal Memory Processing
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Transcranial slow oscillation stimulation during sleep enhances memory consolidation in rats
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Sleep spindles are locally modulated by training on a brain–computer interface
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Sleep disturbances are common in patients with autoimmune encephalitis
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Temporal associations between sleep slow oscillations, spindles and ripples
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- 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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