Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples

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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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(2020) Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples
Open Science Framework, DOI:10.17605/OSF.IO/3HPVR.

https://osf.io/3hpvr/

Article and author information

Author details

Hong-Viet Ngo

Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, Netherlands

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5828-5588
Juergen Fell

Department of Epileptology, University of Bonn, Bonn, Germany

Competing interests
The authors declare that no competing interests exist.
Bernhard Staresina

School of Psychology, University of Birmingham, Birmingham, United Kingdom

For correspondence
b.staresina@bham.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0558-9745

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

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.