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

Research output: Contribution to journalArticle

Authors

  • Til Ole Bergmann
  • Mathilde Bonnefond
  • Roemer van der Meij
  • Lorena Deuker
  • Christian E Elger
  • Nikolai Axmacher
  • Juergen Fell

External organisations

  • School of Psychology, University of Birmingham
  • MRC Cognition and Brain Sciences Unit, Cambridge
  • Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, Institute of Psychology, Christian-Albrechts University of Kiel, 24118 Kiel, Germany, Department of Neurology and Stroke, and Hertie Institute for Clinical Brain Research, and Institute for Medical Psychology and Behavioral Neurobiology, University of Tübingen, 72076 Tübingen, Germany, and bergmann@psychologie.uni-kiel.de.
  • Radboud University Nijmegen, Donders Institute for Brain, Behaviour and Cognition, Nijmegen, Netherlands
  • Department of Epileptology, University of Bonn, D-53105 Bonn, Germany.
  • Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, D-44801 Bochum, Germany; German Center for Neurodegenerative Diseases, D-53175 Bonn, Germany.

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.

Details

Original languageEnglish
Pages (from-to)1679-1686
Number of pages8
JournalNature Neuroscience
Volume18
Issue number11
Publication statusPublished - 21 Nov 2015

Keywords

  • Consolidation, Psychology