Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples
Abstract
Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.
Data availability
Raw EEG data (from NC and HIPP) and all results presented in all figures have been uploaded to the Open Science Framework (DOI: 10.17605/OSF.IO/3HPVR). Furthermore, all Matlab code used for data analysis have been made publicly available on GitHub (https://github.com/episodicmemorylab/Ngo_et_al_eLife2020.git).
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Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripplesOpen Science Framework, DOI:10.17605/OSF.IO/3HPVR.
Article and author information
Author details
Funding
Wellcome (107672/Z/15/Z)
- Bernhard Staresina
Deutsche Forschungsgemeinschaft (SFB1089)
- Juergen Fell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Informed consent was obtained from all patients and the study was approved by the ethics committee of the Medical Faculty of the University of Bonn (reference number 042/16).
Copyright
© 2020, Ngo et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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