A transient postnatal quiescent period precedes emergence of mature cortical dynamics
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.
-
A transient postnatal quiescent period precedes emergence of mature cortical dynamicsDryad Digital Repository, doi:10.5061/dryad.15dv41nxp.
Article and author information
Author details
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.
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.
Metrics
-
- 1,994
- views
-
- 338
- downloads
-
- 15
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Although recent studies suggest that activity in the motor cortex, in addition to generating motor outputs, receives substantial information regarding sensory inputs, it is still unclear how sensory context adjusts the motor commands. Here, we recorded population neural activity in the motor cortex via microelectrode arrays while monkeys performed flexible manual interceptions of moving targets. During this task, which requires predictive sensorimotor control, the activity of most neurons in the motor cortex encoding upcoming movements was influenced by ongoing target motion. Single-trial neural states at the movement onset formed staggered orbital geometries, suggesting that target motion modulates peri-movement activity in an orthogonal manner. This neural geometry was further evaluated with a representational model and recurrent neural networks (RNNs) with task-specific input-output mapping. We propose that the sensorimotor dynamics can be derived from neuronal mixed sensorimotor selectivity and dynamic interaction between modulations.
-
- Neuroscience
This study investigates failures in conscious access resulting from either weak sensory input (perceptual impairments) or unattended input (attentional impairments). Participants viewed a Kanizsa stimulus with or without an illusory triangle within a rapid serial visual presentation of distractor stimuli. We designed a novel Kanizsa stimulus that contained additional ancillary features of different complexity (local contrast and collinearity) that were independently manipulated. Perceptual performance on the Kanizsa stimulus (presence vs. absence of an illusion) was equated between the perceptual (masking) and attentional (attentional blink) manipulation to circumvent common confounds related to conditional differences in task performance. We trained and tested classifiers on electroencephalogram (EEG) data to reflect the processing of specific stimulus features, with increasing levels of complexity. We show that late stages of processing (~200–250 ms), reflecting the integration of complex stimulus features (collinearity, illusory triangle), were impaired by masking but spared by the attentional blink. In contrast, decoding of local contrast (the spatial arrangement of stimulus features) was observed early in time (~80 ms) and was left largely unaffected by either manipulation. These results replicate previous work showing that feedforward processing is largely preserved under both perceptual and attentional impairments. Crucially, however, under matched levels of performance, only attentional impairments left the processing of more complex visual features relatively intact, likely related to spared lateral and local feedback processes during inattention. These findings reveal distinct neural mechanisms associated with perceptual and attentional impairments and thus contribute to a comprehensive understanding of distinct neural stages leading to conscious access.