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

  1. Hong-Viet Ngo
  2. Juergen Fell
  3. Bernhard Staresina  Is a corresponding author
  1. Radboud University Medical Centre, Netherlands
  2. University of Bonn, Germany
  3. University of Birmingham, United Kingdom

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).

The following data sets were generated

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5828-5588
  2. Juergen Fell

    Department of Epileptology, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. 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.
    ORCID icon "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.

Reviewing Editor

  1. Jonas Obleser, University of Lübeck, Germany

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).

Version history

  1. Received: March 17, 2020
  2. Accepted: July 6, 2020
  3. Accepted Manuscript published: July 13, 2020 (version 1)
  4. Version of Record published: July 15, 2020 (version 2)

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.

Metrics

  • 5,513
    views
  • 661
    downloads
  • 97
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Hong-Viet Ngo
  2. Juergen Fell
  3. Bernhard Staresina
(2020)
Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples
eLife 9:e57011.
https://doi.org/10.7554/eLife.57011

Share this article

https://doi.org/10.7554/eLife.57011

Further reading

    1. Neuroscience
    James Malkin, Cian O'Donnell ... Laurence Aitchison
    Research Article

    Biological synaptic transmission is unreliable, and this unreliability likely degrades neural circuit performance. While there are biophysical mechanisms that can increase reliability, for instance by increasing vesicle release probability, these mechanisms cost energy. We examined four such mechanisms along with the associated scaling of the energetic costs. We then embedded these energetic costs for reliability in artificial neural networks (ANNs) with trainable stochastic synapses, and trained these networks on standard image classification tasks. The resulting networks revealed a tradeoff between circuit performance and the energetic cost of synaptic reliability. Additionally, the optimised networks exhibited two testable predictions consistent with pre-existing experimental data. Specifically, synapses with lower variability tended to have (1) higher input firing rates and (2) lower learning rates. Surprisingly, these predictions also arise when synapse statistics are inferred through Bayesian inference. Indeed, we were able to find a formal, theoretical link between the performance-reliability cost tradeoff and Bayesian inference. This connection suggests two incompatible possibilities: evolution may have chanced upon a scheme for implementing Bayesian inference by optimising energy efficiency, or alternatively, energy-efficient synapses may display signatures of Bayesian inference without actually using Bayes to reason about uncertainty.

    1. Neuroscience
    Wenyu Tu, Samuel R Cramer, Nanyin Zhang
    Research Article

    Resting-state brain networks (RSNs) have been widely applied in health and disease, but the interpretation of RSNs in terms of the underlying neural activity is unclear. To address this fundamental question, we conducted simultaneous recordings of whole-brain resting-state functional magnetic resonance imaging (rsfMRI) and electrophysiology signals in two separate brain regions of rats. Our data reveal that for both recording sites, spatial maps derived from band-specific local field potential (LFP) power can account for up to 90% of the spatial variability in RSNs derived from rsfMRI signals. Surprisingly, the time series of LFP band power can only explain to a maximum of 35% of the temporal variance of the local rsfMRI time course from the same site. In addition, regressing out time series of LFP power from rsfMRI signals has minimal impact on the spatial patterns of rsfMRI-based RSNs. This disparity in the spatial and temporal relationships between resting-state electrophysiology and rsfMRI signals suggests that electrophysiological activity alone does not fully explain the effects observed in the rsfMRI signal, implying the existence of an rsfMRI component contributed by ‘electrophysiology-invisible’ signals. These findings offer a novel perspective on our understanding of RSN interpretation.