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...
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2021-07-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/69011 |
id |
doaj-bdc6175043b2408c8b152aba09440128 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT soledaddominguez atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT liangma atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT hanyu atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT gabriellepouchelon atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT christianmayer atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT georgedspyropoulos atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT claudiacea atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT gyorgybuzsaki atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT gordonfishell atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT dionkhodagholy atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT jenniferngelinas atransientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT soledaddominguez transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT liangma transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT hanyu transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT gabriellepouchelon transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT christianmayer transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT georgedspyropoulos transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT claudiacea transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT gyorgybuzsaki transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT gordonfishell transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT dionkhodagholy transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics AT jenniferngelinas transientpostnatalquiescentperiodprecedesemergenceofmaturecorticaldynamics |
_version_ |
1721211091362512896 |