Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep
Open accessAbstract
During systems-level consolidation, mnemonic representations initially reliant on the hippocampus are thought to migrate to neocortical sites for more permanent storage, with an eminent role of sleep for facilitating this information transfer. Mechanistically, consolidation processes have been hypothesized to rely on systematic interactions between the three cardinal neuronal oscillations characterizing non–rapid eye movement (NREM) sleep. Under global control of de- and hyperpolarizing slow oscillations (SOs), sleep spindles may cluster hippocampal ripples for a precisely timed transfer of local information to the neocortex. We used direct intracranial electroencephalogram recordings from human epilepsy patients during natural sleep to test the assumption that SOs, spindles and ripples are functionally coupled in the hippocampus. Employing cross-frequency phase-amplitude coupling analyses, we found that spindles were modulated by the up-state of SOs. Notably, spindles were found to in turn cluster ripples in their troughs, providing fine-tuned temporal frames for the hypothesized transfer of hippocampal memory traces.
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Timing of cue delivery in relation to SOs, spindles, or spindle refractory periods, or phase-coupling of spindles to SO peak or trough may substantially affect the effect of TMR on memory performance.
“timing of cue delivery in relation to SOs, 129 spindles, or spindle refractory periods, respectively, 116,117,127 or the phase-coupling of spindles to the SO peak or trough 125 may substantially affect the effect of TMR on memory performance.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [116]
The Results (Event-locked analysis; page unavailable) show that spindle power varies with SO phase, supporting the phase-coupling part of the citation. The paper does not test TMR cues or whether this coupling affects TMR-related memory performance; the Discussion says whether the observed coupling directly relates to episodic memory remains an open question. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCue delivery during TMR is associated with increased SO power, amplitude and density, increased spindle power and density, and improved SO-spindle coupling, often associated with TMR-induced memory advantage.
“It is associated with increased SO power, amplitude and density, 120,125,128 increased spindle power and density, 116,117,120,128 as well as improved SO-spindle coupling, 120 and these characteristics are often associated with the TMRinduced memory advantage.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [116]
The Results (Event-locked analysis; page unavailable) show increased spindle power during SO up-states and SO–spindle coupling during sleep. The paper does not report TMR cue delivery or show that cues increase SO or spindle measures, improve coupling, or produce a TMR-induced memory advantage. The Discussion explicitly says whether the observed coupling directly relates to episodic memory remains an open question. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIntracranial recordings in human patients and rodents confirmed a triple coupling of oscillations with hippocampal ripples nesting in troughs of spindle oscillation, and spindles nesting in upstates of SOs.
“Indeed, intracranial recordings in human patients and rodents confirmed a triple coupling of oscillations with hippocampal ripples nesting in the troughs of the spindle oscillation, and spindles nesting in the upstates of SOs.58,196,197”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [197]
The Results (Event contingencies) and Discussion report hierarchical SO–spindle–ripple coupling in the human hippocampus: spindles are modulated by SOs, and ripples nest in spindle troughs. The study used intracranial recordings from human epilepsy patients, not rodents; its Discussion says prior rodent studies did not establish this three-way hippocampal coupling. (LLM, conf=0.88)
Experimental — accuracy not yet measuredRipples during SWS tend to nest into the excitable troughs of the spindle oscillation, forming spindle-ripple events.
“Ripples during SWS tend to nest into the excitable troughs of the spindle oscillation thereby forming spindle-ripple events.[195][196][197]”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [197]
The beneficial effect of TMR during non-REM sleep on memory performance is well established across a variety of memory domains.
“The beneficial effect of TMR during non-REM sleep on memory performance is well established across a variety of memory domains, 115 including visuospatial 116-119 and verbal 120,121 declarative memory as well as motor learning.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [116]
The Introduction says NREM sleep facilitates memory consolidation, and the Discussion reports that externally facilitating slow oscillations can boost later retrieval. Neither passage addresses targeted memory reactivation (TMR) or establishes its benefits across memory domains. Searches for TMR, reactivation cues, and the named domains found no passage that verifies the attributed claim. (LLM, conf=0.72)
Experimental — accuracy not yet measured
Covert reactivation of mnemonic content underlies sleep-dependent memory consolidation by propagating information from hippocampal to neocortical regions via a synchronized interplay of hippocampal sharp-wave ripples, thalamic spindles, and neocortical slow waves.
“According to contemporary models and backed by a growing body of research,5,6,7,8 covert reactivation of mnemonic content underlies sleep-dependent memory consolidation by propagating information from hippocampal to neocortical regions via a synchronized interplay of hippocampal sharp-wave ripples, thalamic spindles, and neocortical slow waves.9,10”
From Random auditory stimulation during sleep disturbs traveling slow waves and declarative memory (2026) · cites this paper as [10]
Our findings that auditory stimulation decreased SWS, disrupted slow waves, and impaired declarative memory consolidation support theories of active systems consolidation during sleep, which stress the importance of a coordinated interplay between slow waves, spindles, and ripples for declarative memory processing.
“Taken together, our findings that auditory stimulation decreased SWS, disrupted slow waves, and impaired declarative memory consolidation support theories of active systems consolidation during sleep,9,10 which stress the importance of a coordinated interplay between slow waves, spindles, and ripples for declarative memory processing.”
From Random auditory stimulation during sleep disturbs traveling slow waves and declarative memory (2026) · cites this paper as [10]
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- Authors
- Staresina, B. P., Bergmann, T. O., Bonnefond, M., van der Meij, R., Jensen, O., Deuker, L., Elger, C. E., Axmacher, N., & Fell, J.
- Affiliations
- MRC Cognition and Brain Sciences Unit (GB)
- Radboud University Nijmegen (NL)
- University of Bonn (DE)
- Corresponding author
- Staresina, Bernhard P
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2015-09-21
- Volume
- 18
- Issue
- 11
- Pages
- 1679-1686
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4625581
- OpenAlex
- W2218418953
- Semantic Scholar
- 8874390fcd4d37657b1c4308820582f00899ba34
- Cited by
- 831
- References
- 56
- Citations by year
- 2026: 85 · 2025: 91 · 2024: 92 · 2023: 104 · 2022: 86 · 2021: 75 · 2020: 89 · 2019: 64 · 2018: 53 · 2017: 58 · 2016: 32 · 2015: 2
- FWCI
- 29.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
- DZNE Pub (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- Wellcome Trust (WT089049AIA, 089049)
- Deutsche Forschungsgemeinschaft (SFB1089, AX 82/2, AX82/3)
- Ministerie van Economische Zaken
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (453-09-002)
- 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 spindles, hippocampal ripples, NREM sleep, memory consolidation, cross-frequency coupling, phase-amplitude coupling, intracranial EEG, epilepsy patients, memory reactivation
- MeSH terms
- Adult, Electroencephalography, Epilepsy, Female, Hippocampus, Humans, Male, Memory, Sleep, Neocortex, Young Adult
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