Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings
Open accessAbstract
Sleep spindles are an electroencephalographic (EEG) hallmark of non-rapid eye movement (NREM) sleep and are believed to mediate many sleep-related functions, from memory consolidation to cortical development. Spindles differ in location, frequency, and association with slow waves, but whether this heterogeneity may reflect different physiological processes and potentially serve different functional roles remains unclear. Here we used a unique opportunity to record intracranial depth EEG and single-unit activity in multiple brain regions of neurosurgical patients to better characterize spindle activity in human sleep. We find that spindles occur across multiple neocortical regions, and less frequently also in the parahippocampal gyrus and hippocampus. Most spindles are spatially restricted to specific brain regions. In addition, spindle frequency is topographically organized with a sharp transition around the supplementary motor area between fast (13-15 Hz) centroparietal spindles often occurring with slow-wave up-states, and slow (9-12 Hz) frontal spindles occurring 200 ms later on average. Spindle variability across regions may reflect the underlying thalamocortical projections. We also find that during individual spindles, frequency decreases within and between regions. In addition, deeper NREM sleep is associated with a reduction in spindle occurrence and spindle frequency. Frequency changes between regions, during individual spindles, and across sleep may reflect the same phenomenon, the underlying level of thalamocortical hyperpolarization. Finally, during spindles neuronal firing rates are not consistently modulated, although some neurons exhibit phase-locked discharges. Overall, anatomical considerations can account well for regional spindle characteristics, while variable hyperpolarization levels can explain differences in spindle frequency.
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Fast sleep spindles can reach 18 Hz.
“Frequencies below 20 Hz were avoided because of the potential overlap with fast sleep spindles, which can reach 18 Hz 65,66 .”
From The neural correlates of dreaming (2017) · cites this paper as [65]
The Introduction describes fast spindles as 13–15 Hz, and the Discussion describes them as 13–16 Hz. These passages support the concern about overlap below 20 Hz, but they do not establish that fast spindles can reach 18 Hz. Page numbers were not available in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn the neocortex, single spindles typically express as local phenomena and are restricted to specific regions and circuits, regardless of whether or not they are synchronized in phase with central thalamic spindle generation.
“Importantly, this research revealed that in the neocortex, single spindles typically express as a local phe-nomena and are restricted to specific regions and circuits, regardless of whether or not they are synchronized in phase with central thalamic spindle generation.”
From About Sleep's Role in Memory (2013) · cites this paper as [38]
The Discussion section “Sleep spindles are mostly local” says that most sleep spindles occur locally during natural sleep, supporting the claim that individual neocortical spindles are often regionally restricted. The paper does not establish that this locality holds regardless of phase synchronization with a central thalamic spindle generator; its discussion of spindle synchronization does not test that qualification. Page numbers are unavailable in our copy. (LLM, conf=0.86)
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 [38]
The Results sections ‘Fast centroparietal spindles precede slow frontal spindles’ and ‘Association of spindles with slow wave up-states’ report that fast spindles precede slow frontal spindles by 203 ±16 ms and are more tightly associated with up-states. They do not say that only fast spindles synchronize with up-states. The Discussion section ‘The relation of spindles with sleep slow waves’ says frontal spindles occur later during up-states, not specifically at the up-to-down transition. Page numbers were not available in our copy. (LLM, conf=0.87)
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Research works printed but not linked: 3
- Contreras D Destexhe A Steriade M Spindle oscillations during cortical spreading depression in naturally sleeping cats Neuroscience 1997b 77 933 936 9130774
- Jones EG The thalamus 2007 Cambridge University Press Cambridge, UK; New York 2nd Edition
- Steriade M Neuronal Substrates of Sleep and Epilepsy 2003 Cambridge University Press Cambridge, UK 1st Edition
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“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).”
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“Faster centroparietal spindles begin several hundred milliseconds earlier than slower spindles occurring in frontal cortex [27].”
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Self-citationInterictal epileptiform discharges shape large-scale intercortical communication
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Cortical functional connectivity indexes arousal state during sleep and anesthesia
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Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans
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fMRI spectral signatures of sleep
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Cortical source localization of sleep-stage specific oscillatory activity
Brancaccio, A., Tabarelli, D., Bigica, M., & Baldauf, D. (2020) · Scientific Reports · doi:10.1038/s41598-020-63933-5 · Cited by 60 · see citing works
Nir, Y., Massimini, M., Boly, M., & Tononi, G. (2013) · Springer eBooks · doi:10.1007/978-3-642-37580-4_9 · Cited by 59 · see citing works
Self-citationQuaternion Singular Spectrum Analysis of Electroencephalogram With Application in Sleep Analysis
Enshaeifar, S., Kouchaki, S., Took, C. C., & Sanei, S. (2015) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2015.2465177 · Cited by 60 · see citing works
Sleep Spindles as an Electrographic Element: Description and Automatic Detection Methods
Wallant, D. C. ’., Maquet, P., & Phillips, C. L. M. (2016) · Neural Plasticity · doi:10.1155/2016/6783812 · Cited by 59 · see citing works
- Authors
- Andrillon, T., Nir, Y., Staba, R. J., Ferrarelli, F., Cirelli, C., Tononi, G., & Fried, I.
- Affiliations
- University of Wisconsin–Madison (US)
- University of California, Los Angeles (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-12-07
- Volume
- 31
- Issue
- 49
- Pages
- 17821-17834
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3270580
- OpenAlex
- W2004454719
- Cited by
- 504
- References
- 93
- Citations by year
- 2026: 26 · 2025: 41 · 2024: 37 · 2023: 57 · 2022: 40 · 2021: 30 · 2020: 48 · 2019: 38 · 2018: 38 · 2017: 46 · 2016: 27 · 2015: 25 · 2014: 21 · 2013: 24 · 2012: 6
- FWCI
- 8.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (DP1OD000579)
- National Institute of Neurological Disorders and Stroke (R01NS071048)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Keywords
- sleep spindles, NREM sleep, single-unit activity, supplementary motor area, parahippocampal gyrus, hippocampus, spindle frequency, topographic organization
- MeSH terms
- Action Potentials, Adult, Brain, Brain Mapping, Electroencephalography, Electromyography, Electrooculography, Epilepsy, Female, Humans, Male, Middle Aged, Neurons, Sleep, Spectrum Analysis, Time Factors, Polysomnography, Nonlinear Dynamics, Young Adult, Brain Waves
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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