Fast and Slow Spindles during the Sleep Slow Oscillation: disparate Coalescence and engagement in Memory processing
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STUDY OBJECTIVES: Thalamo-cortical spindles driven by the up-state of neocortical slow (< 1 Hz) oscillations (SOs) represent a candidate mechanism of memory consolidation during sleep. We examined interactions between SOs and spindles in human slow wave sleep, focusing on the presumed existence of 2 kinds of spindles, i.e., slow frontocortical and fast centro-parietal spindles. DESIGN: Two experiments were performed in healthy humans (24.5 ± 0.9 y) investigating undisturbed sleep (Experiment I) and the effects of prior learning (word paired associates) vs. non-learning (Experiment II) on multichannel EEG recordings during sleep. MEASUREMENTS AND RESULTS: Only fast spindles (12-15 Hz) were synchronized to the depolarizing SO up-state. Slow spindles (9-12 Hz) occurred preferentially at the transition into the SO down-state, i.e., during waning depolarization. Slow spindles also revealed a higher probability to follow rather than precede fast spindles. For sequences of individual SOs, fast spindle activity was largest for "initial" SOs, whereas SO amplitude and slow spindle activity were largest for succeeding SOs. Prior learning enhanced this pattern. CONCLUSIONS: The finding that fast and slow spindles occur at different times of the SO cycle points to disparate generating mechanisms for the 2 kinds of spindles. The reported temporal relationships during SO sequences suggest that fast spindles, driven by the SO up-state feed back to enhance the likelihood of succeeding SOs together with slow spindles. By enforcing such SO-spindle cycles, particularly after prior learning, fast spindles possibly play a key role in sleep-dependent memory processing.
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Fine-grained temporal analyses revealed a second type of slow (7-12 Hz) spindle that accompanies the up-to-downstate transition of the SO, shows a more frontal cortical distribution, and is probably of different origin.
“Fine-grained temporal analyses of event patterns revealed a second type of slow (7-12 Hz) spindle that accompanies the up-to-downstate transition of the SO, shows a more frontal cortical distribution, and is probably of different origin.184,185”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [184]
The temporal-analysis results (p. 5) place slow spindles at the transition into the SO down-state and show their strongest modulation in frontal channels. The Discussion (p. 8) describes a frontal cortical maximum and points toward separate generating mechanisms. However, the paper identifies these slow spindles as 9–12 Hz (Spindles, p. 2), not 7–12 Hz. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn 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 [826]
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Experimental — accuracy not yet measuredOnly classic fast spindles display strong phase synchronization with the emergent depolarizing upstate of the slow oscillation; slow frontal spindles tend to follow fast spindles by 200-500 ms and occur in the up-to-down state transition.
“As for spindles, only the classic fast spindles display the strong phase synchronization with the emergent depolarizing upstate of the slow oscillation.Slow frontal spindles, in contrast, tend to follow fast spindles by 200 -500 ms and thus occur already in the up-to-down state transition of the slow oscillation (38,826).”
From About Sleep's Role in Memory (2013) · cites this paper as [826]
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Lutz, N. D., Admard, M., Genzoni, E., Born, J., & Rauss, K. (2021) · SLEEP · doi:10.1093/sleep/zsab056 · Cited by 12 · see citing works
García-Pérez, M. A., Irani, M., Tiznado, V., Bustamante, T., Inostroza, M., Maldonado, P. E., & Valdés, J. L. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.891523 · Cited by 10 · see citing works
Westerberg, C. E., Hawkins, C. A., & Rendon, L. (2018) · Learning & Memory · doi:10.1101/lm.046342.118 · Cited by 2 · see citing works
- Authors
- Mölle, M., Bergmann, T. O., Marshall, L., & Born, J.
- Affiliations
- University of Lübeck (DE)
- University Hospital Schleswig-Holstein (DE)
- Corresponding author
- Mölle, Matthias
- Venue
- Sleep
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-10
- Volume
- 34
- Issue
- 10
- Pages
- 1411-1421
- ISSN
- 0161-8105 (ISSN-L)
- 1550-9109
- PMC
- PMC3174843
- OpenAlex
- W2038369901
- Semantic Scholar
- 13846f6879521f901e94b4c15c32cc7c703f2319
- Cited by
- 557
- References
- 45
- Citations by year
- 2026: 38 · 2025: 53 · 2024: 45 · 2023: 45 · 2022: 63 · 2021: 37 · 2020: 46 · 2019: 43 · 2018: 34 · 2017: 31 · 2016: 36 · 2015: 19 · 2014: 25 · 2013: 28 · 2012: 10
- FWCI
- 10.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- SLEEP (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- sleep spindles, slow oscillations, slow-wave sleep, thalamocortical oscillations, memory consolidation
- MeSH terms
- Adult, Brain, Electroencephalography, Humans, Learning, Male, Memory, Sleep Stages, Polysomnography, Young Adult
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