Abstract

Sleep slow waves are studied for their role in brain plasticity, homeostatic regulation and their changes during aging. Here, we address the possibility that two types of slow waves co-exist in humans. Thirty young and 29 older adults underwent a night of polysomnographic recordings. Using the Transition frequency, slow waves with a slow transition (slow switchers) and with a fast transition (fast switchers) were discovered. Slow switchers had a high EEG connectivity along their depolarization transition while fast switchers had a lower connectivity dynamic and dissipated faster during the night. Aging was associated with lower temporal dissipation of sleep pressure in slow and fast switchers and lower EEG connectivity at the microscale of the oscillations, suggesting a decreased flexibility in the connectivity network of older individuals. Our findings show that two different types of slow waves with possible distinct underlying functions, coexist in the slow wave spectrum.

Data availability

All codes and transformed data used for all the analyses and most specifically to produce all of the figures of the paper can be freely accessible using this link : https://github.com/jmlina/Slow_Wave_Switchers. As requested, the full software licensing will be provided during the review process. We will follow the guidelines you have mentioned as soon as people in charge will be back. All the process will be done for the final version.This information and link was also added in a new section at the end of the paper under "Additional data files".Dataset can not be shared as participants did not give consent for data sharing.For the raw data, a request needs to be formulated to the ethic committee of the Hôpital de Sacré-Coeur de Montréal, as raw data of human participants cannot be made public under Québec's law.The data provided will be anonymized and some will be processed. Researchers who request access to the data will need to provide their research protocol and their IRB approval for this protocol. The documents will be studied by the owner of the database (Julie Carrier) who will then also submit to her institution's REB for authorization to share the data. Data requests should be addressed to:Julie Carrier (PI): julie.carrier.1@umontreal.caSonia Frenette (in cc) : sonia.frenette@umontreal.ca

Article and author information

Author details

  1. Maude Bouchard

    psychology, Université de Montréal, Montreal, Canada
    For correspondence
    maude.bouchard.1@umontreal.ca
    Competing interests
    The authors declare that no competing interests exist.
  2. Jean-Marc Lina

    Mathematics, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Pierre-Olivier Gaudreault

    Psychology, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandre Lafrenière

    Psychology, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Jonathan Dubé

    Psychology, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Nadia Gosselin

    Psychology, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Julie Carrier

    Psychology, Université de Montréal, Montreal, Canada
    For correspondence
    julie.carrier.1@umontreal.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9863-4436

Funding

Canadian Institutes of Health Research (Vanier scholarship)

  • Maude Bouchard

Canadian Institutes of Health Research (190750)

  • Julie Carrier

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Bryce A Mander, University of California, Irvine, United States

Ethics

Human subjects: The protocol was approved by the ethics committee of the Hôpital du Sacré-Coeur de Montréal and performed in accordance with the relevant guidelines and regulations. Participants provided informed consent and received financial compensation for their participation. (CMER-RNQ 08-136 08-002).

Version history

  1. Received: October 26, 2020
  2. Preprint posted: February 3, 2021 (view preprint)
  3. Accepted: August 26, 2021
  4. Accepted Manuscript published: August 27, 2021 (version 1)
  5. Version of Record published: September 20, 2021 (version 2)

Copyright

© 2021, Bouchard 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

  • 1,668
    views
  • 220
    downloads
  • 12
    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. Maude Bouchard
  2. Jean-Marc Lina
  3. Pierre-Olivier Gaudreault
  4. Alexandre Lafrenière
  5. Jonathan Dubé
  6. Nadia Gosselin
  7. Julie Carrier
(2021)
Sleeping at the Switch
eLife 10:e64337.
https://doi.org/10.7554/eLife.64337

Share this article

https://doi.org/10.7554/eLife.64337

Further reading

    1. Neuroscience
    Alexandra L Jellinger, Rebecca L Suthard ... Steve Ramirez
    Research Article

    Negative memories engage a brain and body-wide stress response in humans that can alter cognition and behavior. Prolonged stress responses induce maladaptive cellular, circuit, and systems-level changes that can lead to pathological brain states and corresponding disorders in which mood and memory are affected. However, it is unclear if repeated activation of cells processing negative memories induces similar phenotypes in mice. In this study, we used an activity-dependent tagging method to access neuronal ensembles and assess their molecular characteristics. Sequencing memory engrams in mice revealed that positive (male-to-female exposure) and negative (foot shock) cells upregulated genes linked to anti- and pro-inflammatory responses, respectively. To investigate the impact of persistent activation of negative engrams, we chemogenetically activated them in the ventral hippocampus over 3 months and conducted anxiety and memory-related tests. Negative engram activation increased anxiety behaviors in both 6- and 14-month-old mice, reduced spatial working memory in older mice, impaired fear extinction in younger mice, and heightened fear generalization in both age groups. Immunohistochemistry revealed changes in microglial and astrocytic structure and number in the hippocampus. In summary, repeated activation of negative memories induces lasting cellular and behavioral abnormalities in mice, offering insights into the negative effects of chronic negative thinking-like behaviors on human health.

    1. Neuroscience
    Alexandra H Leighton, Juliette E Cheyne, Christian Lohmann
    Research Article

    Synaptic inputs to cortical neurons are highly structured in adult sensory systems, such that neighboring synapses along dendrites are activated by similar stimuli. This organization of synaptic inputs, called synaptic clustering, is required for high-fidelity signal processing, and clustered synapses can already be observed before eye opening. However, how clustered inputs emerge during development is unknown. Here, we employed concurrent in vivo whole-cell patch-clamp and dendritic calcium imaging to map spontaneous synaptic inputs to dendrites of layer 2/3 neurons in the mouse primary visual cortex during the second postnatal week until eye opening. We found that the number of functional synapses and the frequency of transmission events increase several fold during this developmental period. At the beginning of the second postnatal week, synapses assemble specifically in confined dendritic segments, whereas other segments are devoid of synapses. By the end of the second postnatal week, just before eye opening, dendrites are almost entirely covered by domains of co-active synapses. Finally, co-activity with their neighbor synapses correlates with synaptic stabilization and potentiation. Thus, clustered synapses form in distinct functional domains presumably to equip dendrites with computational modules for high-capacity sensory processing when the eyes open.