A transient postnatal quiescent period precedes emergence of mature cortical dynamics
- Columbia University, United States
- Harvard University, United States
- Max Planck, Germany
- New York University, United States
- 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.
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A transient postnatal quiescent period precedes emergence of mature cortical dynamicsDryad Digital Repository, doi:10.5061/dryad.15dv41nxp.
Article and author information
Author details
Jennifer N Gelinas
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.
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.
Reviewing Editor
- Sacha B Nelson, Brandeis University, United States
Publication history
- Preprint posted: February 17, 2021 (view preprint)
- Received: April 1, 2021
- Accepted: June 26, 2021
- Accepted Manuscript published: July 23, 2021 (version 1)
- 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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A transient postnatal quiescent period precedes emergence of mature cortical dynamics
eLife 10:e69011.
https://doi.org/10.7554/eLife.69011
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