A transient postnatal quiescent period precedes emergence of mature cortical dynamics

Author:

Domínguez Soledad1ORCID,Ma Liang12ORCID,Yu Han3ORCID,Pouchelon Gabrielle4,Mayer Christian5,Spyropoulos George D3,Cea Claudia3,Buzsáki György67ORCID,Fishell Gordon48ORCID,Khodagholy Dion3,Gelinas Jennifer N129ORCID

Affiliation:

1. Institute for Genomic Medicine, Columbia University Medical Center, New York, United States

2. Department of Biomedical Engineering, Columbia University, New York, United States

3. Department of Electrical Engineering, Columbia University, New York, United States

4. The Stanley Center at the Broad, Cambridge, United States

5. Max Planck Institute of Neurobiology, Martinsried, Germany

6. Neuroscience Institute and Department of Neurology New York University Langone Medical Center, New York, United States

7. Center for Neural Science, New York University, New York, United States

8. Department of Neurobiology, Harvard Medical School, Boston, United States

9. Department of Neurology, Columbia University Medical Center, New York, 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.

Funder

National Institutes of Health

H2020 European Research Council

NSF

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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