A transient postnatal quiescent period precedes emergence of mature cortical dynamics

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. W...

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Main Authors: Soledad Domínguez, Liang Ma, Han Yu, Gabrielle Pouchelon, Christian Mayer, George D Spyropoulos, Claudia Cea, György Buzsáki, Gordon Fishell, Dion Khodagholy, Jennifer N Gelinas
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/69011
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spelling doaj-bdc6175043b2408c8b152aba094401282021-08-11T13:20:29ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.69011A transient postnatal quiescent period precedes emergence of mature cortical dynamicsSoledad Domínguez0https://orcid.org/0000-0003-0378-2442Liang Ma1https://orcid.org/0000-0003-3883-1902Han Yu2https://orcid.org/0000-0002-7110-7716Gabrielle Pouchelon3Christian Mayer4George D Spyropoulos5Claudia Cea6György Buzsáki7https://orcid.org/0000-0002-3100-4800Gordon Fishell8https://orcid.org/0000-0002-9640-9278Dion Khodagholy9Jennifer N Gelinas10https://orcid.org/0000-0002-1164-638XInstitute for Genomic Medicine, Columbia University Medical Center, New York, United StatesInstitute for Genomic Medicine, Columbia University Medical Center, New York, United States; Department of Biomedical Engineering, Columbia University, New York, United StatesDepartment of Electrical Engineering, Columbia University, New York, United StatesThe Stanley Center at the Broad, Cambridge, United StatesMax Planck Institute of Neurobiology, Martinsried, GermanyDepartment of Electrical Engineering, Columbia University, New York, United StatesDepartment of Electrical Engineering, Columbia University, New York, United StatesNeuroscience Institute and Department of Neurology New York University Langone Medical Center, New York, United States; Center for Neural Science, New York University, New York, United StatesThe Stanley Center at the Broad, Cambridge, United States; Department of Neurobiology, Harvard Medical School, Boston, United StatesDepartment of Electrical Engineering, Columbia University, New York, United StatesInstitute for Genomic Medicine, Columbia University Medical Center, New York, United States; Department of Biomedical Engineering, Columbia University, New York, United States; Department of Neurology, Columbia University Medical Center, New York, United StatesMature 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.https://elifesciences.org/articles/69011systems neuroscienceelarge scale electrophysiologycortical development
collection DOAJ
language English
format Article
sources DOAJ
author Soledad Domínguez
Liang Ma
Han Yu
Gabrielle Pouchelon
Christian Mayer
George D Spyropoulos
Claudia Cea
György Buzsáki
Gordon Fishell
Dion Khodagholy
Jennifer N Gelinas
spellingShingle Soledad Domínguez
Liang Ma
Han Yu
Gabrielle Pouchelon
Christian Mayer
George D Spyropoulos
Claudia Cea
György Buzsáki
Gordon Fishell
Dion Khodagholy
Jennifer N Gelinas
A transient postnatal quiescent period precedes emergence of mature cortical dynamics
eLife
systems neuroscience
elarge scale electrophysiology
cortical development
author_facet Soledad Domínguez
Liang Ma
Han Yu
Gabrielle Pouchelon
Christian Mayer
George D Spyropoulos
Claudia Cea
György Buzsáki
Gordon Fishell
Dion Khodagholy
Jennifer N Gelinas
author_sort Soledad Domínguez
title A transient postnatal quiescent period precedes emergence of mature cortical dynamics
title_short A transient postnatal quiescent period precedes emergence of mature cortical dynamics
title_full A transient postnatal quiescent period precedes emergence of mature cortical dynamics
title_fullStr A transient postnatal quiescent period precedes emergence of mature cortical dynamics
title_full_unstemmed A transient postnatal quiescent period precedes emergence of mature cortical dynamics
title_sort transient postnatal quiescent period precedes emergence of mature cortical dynamics
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-07-01
description 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.
topic systems neuroscience
elarge scale electrophysiology
cortical development
url https://elifesciences.org/articles/69011
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