Three Patterns of Oscillatory Activity Differentially Synchronize Developing Neocortical Networks In Vivo

Properties of spindle bursts, gamma oscillations, and long oscillations. A, Characteristic spindle burst recorded in S1 of a P1 rat (top) and corresponding MUA after 200 Hz high-pass filtering (below). Note the correlation between spindle burst and MUA. Color-coded frequency plot shows the wavelet spectrum of the field potential recording at identical timescale. Fast Fourier transformation (FFT) of the field potential recording illustrating the relative power of the displayed spindle burst with a maximal frequency at 10 Hz (bottom). B, Characteristic gamma oscillation (top) recorded in the S1 of a P3 rat and corresponding MUA (below). Wavelet and FFT spectrum reveal prominent gamma activity between 30 and 50 Hz. C, Characteristic long oscillation (top) recorded in S1 of a P6 rat and corresponding MUA (below). Color-coded wavelet spectrum and FFT (bottom) of the field potential recording display a narrow peak at 23 Hz. Note strong MUA at the onset of the long oscillation and different timescale compared with A and B.

Spatiotemporal properties and developmental profile of spindle burst activity in neonatal rat S1. A, Spatial distribution of spindle bursts recorded at 94 recording sites in 50 P0–P7 rats. The stereotaxic coordinates of the recording sites were determined in relationship to bregma and midline in each pup and are displayed normalized to the lateral and posterior borders (100%) of the barrel field (light blue). The occurrence (i), amplitude (ii), duration (iii), and maximal frequency within burst (iv) of each spindle burst were normalized to the maximal value and displayed in color code. Spindle bursts recorded within the barrel field revealed a higher occurrence, larger amplitude, lower duration, and higher frequency when compared with spindle bursts recorded outside the barrel field. B, Developmental profile of the spindle burst activity in P0–P7 rat S1. Box plots displaying the progressive increase in the occurrence (i), amplitude (ii), and maximal frequency within burst (iv) during the first postnatal week. The average spindle burst duration reveals no major change during early development (iii). C, Spindle bursts gradually shift toward faster frequency bands with a relatively stable contribution of alpha activity. In B and C, the values correspond to spindle bursts recorded from 10 P0–P1 pups, 16 P2–P3 pups, 12 P4–P5 pups, and 12 P6–P7 pups. Data are expressed as box plots, and asterisks mark significant differences compared with the P0–P1 group (*p < 0.05, **p < 0.01, ***p < 0.001, Mann–Whitney–Wilcoxon test).

Intrahemispheric and interhemispheric synchronization of spindle bursts in the neonatal rat barrel cortex. A, i, Simultaneous field potential recordings from a P1 rat with the 4 × 4-channels electrode array (interelectrode distance of 200 μm) demonstrating simultaneous spindle burst activity at multiple recording sites. ii, Color-coded plots of maximal cross-correlation and coherence coefficients calculated for the 4 × 4 recordings shown in i. Channel number 14 (red box in i and × in plots) was used as reference channel, and the coherence was calculated for the dominant alpha frequency band. Note the columnar-like distribution of the significant cross-correlation and coherence coefficients marked by asterisks. B, i, Digital photomontage of a 200-μm-thick Nissl-stained coronal slice reconstructing the position of the two DiI-covered 4 × 4-channels electrode arrays inserted at the same stereotaxic coordinates in both hemispheres of a P7 rat. ii, Simultaneous field potential recordings from the upper channels of the electrode arrays (marked by red boxes in i). Note synchronized spindle bursts activity at homotopic recording sites in both hemispheres (channel 1 left vs channel 13 right hemisphere). The red dotted line marks the onset of interhemispheric spindle bursts. iii, Age-dependent increase in interhemispheric synchronization of spindle burst activity from P0 to P7 in rat barrel cortex. Box plot displaying the relative amount of spindle bursts occurring simultaneously on both hemispheres in relationship to the total amount of spindle bursts. The displayed values were obtained in 4 P0–P1 pups, 7 P2–P3 pups, 6 P4–P5 pups, and 10 P6–P7 pups.

Spatiotemporal properties and developmental profile of gamma oscillations. A, Spatial distribution of gamma activity recorded at 54 recording sites in 32 newborn rats. Note that gamma oscillations are mainly restricted to the cortical region corresponding to the barrel field in S1. Open circles correspond to stereotaxic coordinates in which gamma oscillations could not be recorded. B, Developmental profile of the gamma oscillations in P0–P7 rat S1. Box plots illustrate age-dependent alterations in the occurrence (i), amplitude (ii), duration (iii), and maximal frequency (iv) during the first postnatal week. The displayed values correspond to gamma oscillations recorded in 5 P0–P1 pups, 8 P2–P3 pups, 8 P4–P5 pups, and 11 P6–P7 pups. For additional details, see Figure 3.

Intrahemispheric and interhemispheric synchronization of gamma oscillations. A, i, Simultaneous field potential recordings in a P3 rat somatosensory cortex showing gamma oscillations at a few recording sites. ii, Color-coded plot of maximal cross-correlation coefficients calculated for the 16 recordings shown in i with channel 9 as a reference channel (red box in i). Note spatial restriction of synchronized gamma activity to only two recording sites. B, Simultaneous gamma oscillations recorded at homotopic sites in left and right hemispheres in a P3 rat. The red dotted line marks the onset of synchronized interhemispheric gamma oscillations. C, Incidence of interhemispheric gamma synchronization during the first postnatal week. The values correspond to gamma oscillations recorded in five P0–P2 pups, eight P3–P5 pups, and seven P6–P7 pups.

Spatiotemporal properties and developmental profile of long oscillations. A, Spatial distribution of long oscillations recorded at 24 recording sites in 20 newborn rats. Note the relatively low incidence of long oscillations in the barrel field. B, Developmental profile of long oscillations in P0–P7 rat S1. Box plots illustrate age-dependent alterations in the occurrence (i), amplitude (ii), duration (iii), and maximal frequency (iv) during the first postnatal week. Long oscillations reveal a significant increase in frequency during the first postnatal week. The values correspond to long oscillations recorded in six P0–P1 pups, seven P2–P3 pups, three P4–P5 pups, and four P6-P7 pups. For additional details, see Figure 3.

Synchronization and horizontal propagation of long oscillations. A, i, Simultaneous recordings of long oscillations in the barrel cortex of a P6 rat. Note prominent expression of long oscillations at all recording sites. ii, Color-coded plot of maximal cross-correlation and coherence coefficients calculated for the 16 recordings shown in i using channel 5 (red box in i, and × in ii) as a reference channel. The coherence was calculated for the dominant beta frequency band. Note the wide-spread synchronization of long oscillations as indicated by the large number of recording sites with high cross-correlation and coherence coefficients. B, Simultaneous recordings of long oscillations at four recording sites located at the same cortical depth in the barrel field of a P6 rat.