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Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep

Nature Neuroscience volume 18, pages 16791686 (2015) | Download Citation

Abstract

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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Acknowledgements

The research was supported by a Sir Henry Wellcome Fellowship (WT089049AIA) to B.P.S., the BrainGain Smart Mix Programme of the Netherlands Ministry of Economic Affairs (T.O.B.), the VICI grant (453-09-002) from the NWO (O.J.) and the DFG grants AX82/2, AX82/3 (N.A.) and SFB1089 (N.A. and J.F.).

Author information

Author notes

    • Bernhard P Staresina
    •  & Til Ole Bergmann

    These authors contributed equally to this work.

Affiliations

  1. School of Psychology, University of Birmingham, Birmingham, UK.

    • Bernhard P Staresina
  2. MRC Cognition and Brain Sciences Unit, Cambridge, UK.

    • Bernhard P Staresina
  3. Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, the Netherlands.

    • Til Ole Bergmann
    • , Mathilde Bonnefond
    • , Roemer van der Meij
    • , Ole Jensen
    •  & Lorena Deuker
  4. Institute of Psychology, Christian-Albrechts-University of Kiel, Kiel, Germany.

    • Til Ole Bergmann
  5. Department of Neurology and Stroke, and Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

    • Til Ole Bergmann
  6. Institute for Medical Psychology and Behavioral Neurobiology, University of Tübingen, Tübingen, Germany.

    • Til Ole Bergmann
  7. Department of Epileptology, University of Bonn, Bonn, Germany.

    • Christian E Elger
    • , Nikolai Axmacher
    •  & Juergen Fell
  8. German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.

    • Nikolai Axmacher
  9. Department of Neuropsychology, Institute of Cognitive Neuroscience, Ruhr University Bochum, Bochum, Germany.

    • Nikolai Axmacher

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Contributions

B.P.S. and T.O.B. analyzed the data. B.P.S., T.O.B. and J.F. wrote the manuscript. L.D. acquired data. B.P.S., T.O.B., M.B., R.v.d.M., O.J., N.A. and J.F. provided analytical tools. C.E.E. supervised intracranial recordings.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Bernhard P Staresina.

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DOI

https://doi.org/10.1038/nn.4119

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