A transient postnatal quiescent period precedes emergence of mature cortical dynamics

  1. Soledad Dominguez
  2. Liang Ma
  3. Han Yu
  4. Gabrielle Pouchelon
  5. Christian Mayer
  6. George D Spyropoulos
  7. Claudia Cea
  8. György Buzsáki
  9. Gordon Fishell
  10. Dion Khodagholy  Is a corresponding author
  11. Jennifer N Gelinas  Is a corresponding author
  1. Columbia University, United States
  2. Harvard University, United States
  3. Max Planck, Germany
  4. New York University, United States
  5. Harvard Medical School, United States

Abstract

Mature neural networks synchronize and integrate spatiotemporal activity patterns to support cognition. Emergence of these activity patterns and functions is believed to be developmentally regulated, but the postnatal time course for neural networks to perform complex computations remains unknown. We investigate the progression of large-scale synaptic and cellular activity patterns across development using high spatiotemporal resolution in vivo electrophysiology in immature mice. We reveal that mature cortical processes emerge rapidly and simultaneously after a discrete but volatile transition period at the beginning of the second postnatal week of rodent development. The transition is characterized by relative neural quiescence, after which spatially distributed, temporally precise, and internally organized activity occurs. We demonstrate a similar developmental trajectory in humans, suggesting an evolutionarily conserved mechanism that could facilitate a transition in network operation. We hypothesize that this transient quiescent period is a requisite for the subsequent emergence of coordinated cortical networks.

Data availability

Source data are presented in Supplementary Figures and uploaded to Dryad. Data pertaining to human subjects is governed by IRB policy and can be accessed through application to the IRB. Pooled, processed human subject data are uploaded to Dryad.

The following data sets were generated

Article and author information

Author details

  1. Soledad Dominguez

    Neurology, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Liang Ma

    Biomedical Engineering, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Han Yu

    Electrical Engineering, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Gabrielle Pouchelon

    Neurobiology, Harvard University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Christian Mayer

    Neurobiology, Max Planck, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. George D Spyropoulos

    Electrical Engineering, Columbia University, new York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Claudia Cea

    Electrical Engineering, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. György Buzsáki

    Neuroscience Institute, Langone Medical Center, Department of Neurology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3100-4800
  9. Gordon Fishell

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9640-9278
  10. Dion Khodagholy

    Electrical Engineering, Columbia University, New York, United States
    For correspondence
    dk2955@Columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. Jennifer N Gelinas

    Neurology, Columbia University, New York, United States
    For correspondence
    jng2146@cumc.columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1164-638X

Funding

National Institutes of Health (R21 EY032381)

  • Dion Khodagholy
  • Jennifer N Gelinas

H2020 European Research Council (Marie Skłodowska-Curie grant agreement No 799501)

  • Soledad Dominguez

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

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Ethics

Animal experimentation: All animal experiments were performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health and approved by the Institutional Animal Care and Use Committee at Columbia University Irving Medical Center.protocol AABI5568.

Human subjects: We retrospectively analyzed EEG recordings from 54 patients who underwent continuous monitoring with surface electroencephalography (EEG) as part of clinical diagnostic assessment. Analysis of these data were approved by the Institutional Review Board at Columbia University Irving Medical Center, and all data collection occurred at this institution. All data reviewed was initially obtained for clinical management purposes and informed consent was waived as per 45 CFR 46.116.

Version history

  1. Preprint posted: February 17, 2021 (view preprint)
  2. Received: April 1, 2021
  3. Accepted: June 26, 2021
  4. Accepted Manuscript published: July 23, 2021 (version 1)
  5. Version of Record published: August 11, 2021 (version 2)

Copyright

© 2021, Dominguez 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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  1. Soledad Dominguez
  2. Liang Ma
  3. Han Yu
  4. Gabrielle Pouchelon
  5. Christian Mayer
  6. George D Spyropoulos
  7. Claudia Cea
  8. György Buzsáki
  9. Gordon Fishell
  10. Dion Khodagholy
  11. Jennifer N Gelinas
(2021)
A transient postnatal quiescent period precedes emergence of mature cortical dynamics
eLife 10:e69011.
https://doi.org/10.7554/eLife.69011

Share this article

https://doi.org/10.7554/eLife.69011

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