A transient postnatal quiescent period precedes emergence of mature cortical dynamics
- Institute for Genomic Medicine, Columbia University Medical Center, United States
- Department of Biomedical Engineering, Columbia University, United States
- Department of Electrical Engineering, Columbia University, United States
- The Stanley Center at the Broad, United States
- Max Planck Institute of Neurobiology, Germany
- Neuroscience Institute and Department of Neurology New York University Langone Medical Center, United States
- Center for Neural Science, New York University, United States
- Department of Neurobiology, Harvard Medical School, United States
- Department of Neurology, Columbia University Medical Center, United States
Figures
Figure 1 with 5 supplements
Large-scale, high spatiotemporal resolution recording of neural activity across development in rodents demonstrates conserved features with human electroencephalography (EEG).
(A) Optical micrograph of NeuroGrid conforming to the surface of a P7 mouse pup (upper; scale bar 200 µm). Optical micrograph revealing arrangement of electrodes and perforations in section of …
Figure 1—figure supplement 1
Neurophysiological recording in mouse pups.
(A) Customized surgical set-up with P7 pup for scale. (B) Schematic of neurophysiological recording set-up with continuous recording of electromyography (EMG) and electrocardiography (ECG), control …
Figure 1—figure supplement 2
Recovery of spindle band oscillation occurrence rate and neural spiking after anesthesia for neural interface device placement.
(A) Normalized spindle band oscillation occurrence rate increases after anesthesia and stabilizes. Asterisks represent timepoint after which data was used for neural analysis. (B) Spindle band …
Figure 1—figure supplement 3
Histological processing and anatomical localization of NeuroGrid electrodes.
(A) Schematic demonstrating flattening of cortical mantle for immunohistochemical processing. (B) Reconstruction of NeuroGrid location using chitosan marking (green) relative to somatosensory and …
Figure 1—figure supplement 4
Localized neural spiking across cortical layers.
Sample raw traces spanning cortical layers (black; upper = most superficial, lower = deepest) in a P13 mouse pup. Corresponding electrocardiography (blue, upper) and electromyography traces (blue, …
Figure 1—figure supplement 5
Isolation of putative quiet/non-rapid eye movement (NREM) epochs in mouse pups.
(A) Three sample raw traces from P7 mouse pup (black) and high-pass filtered electromyography (EMG) trace (red). Green shaded area indicates epoch of muscle atonia lasting > 10 s, consistent with …
Figure 2 with 4 supplements
Duration and power of cortical oscillatory activity transiently decreases at the beginning of the second postnatal week.
(A) Sample raw NeuroGrid traces from P5–14 mouse pups demonstrating changing characteristics of oscillatory patterns across development with relative paucity of activity at P8 and P9 (shaded gray …
Figure 2—figure supplement 1
Average power spectra across development.
Spectral power in P8–9 pups is low power with a paucity of well-defined peaks (n = 51 pups, solid line = mean, shaded error bars = ±SE).
Figure 2—figure supplement 2
Model fitting and selection with bootstrapping to identify local minima.
(A) Datapoints from Figure 2C (gray circles) with superimposed regression models (linear, second- to sixth-order polynomials). (B) Leave-one-out cross-validation to evaluate fit of each model …
Figure 2—figure supplement 3
Model selection and verification of nonlinear developmental trajectory for wideband power in mice.
Leave-one-out cross-validation to evaluate fit of each model for wideband power, quantified by mean squared error (left). Plot of residuals obtained from linear regression fitting (right); note …
Figure 2—figure supplement 4
Quantification of sleep proportion and twitch rate in mouse pups.
(A) The proportion of putative active relative to quiet sleep decreased gradually with maturation (n = 47 pups, p=0.0002; post-hoc testing reveals significant difference between P5–7 and P10–12 …
Figure 3 with 2 supplements
Rate and temporal precision of neural spiking increase after the beginning of the second postnatal week.
(A) Neural spiking rate (layers IV–VI) increases nonlinearly across development (blue line = mean; shaded blue areas ± SE) with a local minimum at the beginning of the second postnatal week (n = 38 …
Figure 3—figure supplement 1
Bootstrapping, model selection and verification of nonlinear developmental trajectory for spiking recruitment to neural spiking rate in mice.
(A) Comparison of nadir localization from distributions obtained by bootstrapping across ages (gray) and within ages (orange) revealing significantly increased probability of local minimum at the …
Figure 3—figure supplement 2
Bootstrapping, model selection and verification of nonlinear developmental trajectory for spiking recruitment to inter-spike interval in mice.
(A) Comparison of nadir localization from distributions obtained by bootstrapping across ages (gray) and within ages (orange) revealing significantly increased probability of local maximum at the …
Figure 4 with 1 supplement
Key functional oscillatory properties transition at the beginning of the second postnatal week.
(A) Magnitude and variability of spindle band oscillation spatial extent varies across pup development (n = 44 pups, 42,335 spindle band oscillations; Kolmogorov–Smirnov [KS] statistic P5 vs. P8 = …
Figure 4—figure supplement 1
Model selection and verification of nonlinear developmental trajectory for spindle band oscillation properties in mice.
Leave-one-out cross-validation to evaluate fit of each model for spindle band oscillation properties, quantified by mean squared error (left). Plot of residuals obtained from linear regression …
Figure 5 with 1 supplement
Increasing regularity and temporal precision of synaptic activity facilitates recruitment and entrainment of neural spiking across development.
(A) Frequency comodulation at the time of spindle band oscillations emerges across development. Comodulograms (upper) and quantification of significant peaks in frequency coherence to spindle band …
Figure 5—figure supplement 1
Bootstrapping, model selection and verification of nonlinear developmental trajectory for spiking recruitment to spindle band oscillations in mice.
(A) Comparison of nadir localization from distributions obtained by bootstrapping across ages (gray) and within ages (orange) revealing significantly increased probability of local minimum at the …
Figure 6 with 3 supplements
A transient quiescent state shifts network dynamics in humans.
(A) Sample raw traces from human subjects revealing a relative paucity of activity between 42 and 47 weeks during quiet/non-rapid eye movement (NREM) sleep (gray shaded box). Orange shaded box is …
Figure 6—figure supplement 1
Demographic characteristics of human subjects.
(A) Histogram of age at birth. (B) Histogram of age at time of continuous electroencephalography (EEG) monitoring. (C) Clinical indication for continuous EEG monitoring (BRUE: brief resolved …
Figure 6—figure supplement 2
Bootstrapping, model selection and verification of nonlinear developmental trajectory for continuity, wideband power, and spatial extent of spindle band oscillations in human subjects.
(A) Comparison of nadir localization from distributions obtained by bootstrapping across ages (gray) and within ages (orange) revealing significantly increased probability of local minimum between …
Figure 6—figure supplement 3
Spectral features and power law characteristics in human subjects.
(A) Sample power spectrum from 36-week post-gestation subject. Dashed line models the aperiodic component of the power spectrum. (B) Sample power spectrum from 43-week post-gestation subject. Dashed …
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Strain, strain background (Mus musculus) | SW (Crl:CFW) | Charles River | IMSR Cat# CRL:024, RRID:IMSR_CRL:024 | Mouse |
| Antibody | Anti-VGLUT2 (polyclonal; target: mouse, rat; host: guinea pig) | Synaptic Systems | Cat# 135 404, RRID:AB_887884 | Primary antibody, dilution 1:1000 |
| Antibody | 594 Donkey Anti-Guinea Pig IgG (H+L) (polyclonal; target: guinea pig; host: donkey) | Jackson ImmunoResearch Labs | Cat# 706-585-148, RRID:AB_2340474 | Secondary antibody, dilution 1:500 |
| Software, algorithm | MATLAB | MathWorks | RRID:SCR_001622 | |
| Software, algorithm | Chronux | Chronux.org | RRID:SCR_005547 |
