γ- and β-Oscillations during sleep and wakefulness. (A) γ- and β-oscillations were identified in LFPs during SWS and wakefulness (Wake) in both human and monkey. The raw and filtered traces (Top) and wavelet time frequency of the sample epoch (Bottom) are shown. Chan, channel. (B) These oscillations most frequently appeared at about the same time across the array, forming broad spatial patterns. Red and blue dots are spiking from inhibitory FS and excitatory RS cells recorded with the same electrodes from which the LFP oscillatory envelope is calculated.

γ- and β-Oscillations during sleep and wakefulness. (A) Recordings from (4 × 4 mm) 100-electrode Utah (Neuroprobe) arrays are shown for neocortical γ-oscillations in the temporal lobe of humans (Left) and β-oscillations in the PMd and MI of monkey (Right). (Left) Array is implanted using a pneumatic device (blue arrow) under an ECoG macrogrid. Histology shows that the array tract penetrates at least as far as superficial layer III (arrows). Glial fibrillary acidic protein staining highlights focal gliosis of the superficial layers of the cortex. Neuronal specific nuclear protein immunohistochemical staining reveals normal cortical layering with no evidence of cortical dysplasia. (Right) Sleep recordings were from PMd and MI arrays, and not a ventral premotor (PMv) array. The scale of the array is shown on the far right against the fingertip. (B) Power spectra of a few hundred examples of high-frequency oscillations during recorded vigilance states. Each column of the color-coded matrix is the average of time frequency during an example epoch. WAKE, wakefulness.

Examples of neocortical γ-events in sleep. (Top) Example γ-events from human patient 1. In these heat maps, each row is a different LFP channel (Chan). Red and blue dots show spiking activity of FS and RS cells, localized at the same electrodes that were used to record the LFPs. (Middle) Raw traces of average LFP recordings. (Bottom) Wavelet time frequency (TF) of the average LFP.

Examples of neocortical β-events in sleep. (Top) Example β-events from monkey. In these heat maps, each row is a different LFP channel. Red and blue dots show spiking activity of FS and RS cells, localized at the same electrodes that were used to record the LFPs. (Middle) Raw traces of average LFP recordings. (Bottom) Wavelet time frequency of the average LFP.

Oscillation-triggered probability density of firing rates for RS and FS neurons. In each triplet set of heat maps, one shows wavelet time frequency (Bottom) and the other two show FS (Top) and RS (Middle) firing during these example γ- and β-oscillations. The firing rate is color-coded [black, baseline firing rate; white, 5 standard deviations (std) from the baseline]. The cells are ordered by their discharge probability during γ- or β-oscillation (20-ms bin size). A large proportion of FS cells show an increased firing rate during γ and β. Raster plots show spiking patterns of a few sample FS and RS cells. In these raster plots, each row is the spiking of the example cell in one (γ or β) oscillatory epoch. The corresponding average firing pattern (rows in the heat map) for each example cell (FS1, RS2, etc.) is indicated along the right edge of the heat maps. Note the remarkably heterogeneous discharge patterns.

Phase-locking of spikes relative to the field oscillation cycle for RS and FS neurons during SWS. Phase-locking was considered significant if the hypothesis of circular uniformity for its field phase distribution could be rejected at P = 0.05 using a Rayleigh statistical test. (A) Phase distributions of several significantly phase-locked RS and FS cells. The distributions were fitted with a von Mises function depicted here with continuous black lines. rad, radian. (B) Histogram of Rayleigh’s Z value for all investigated RS (blue) and FS (red) cells. Note the large proportion of FS cells that were modulated by β and γ patterns. (C) Histograms of preferred firing phase for significantly phase-locked neurons. For each RS (blue) and FS (red) cell, the normalized distribution is depicted (hot colors), with black dots indicating the preferred firing phase. Note that, on average, FS cells fired earlier than RS cells.

Oscillation-spiking relation. In this example, ∼700 oscillatory events from a given channel were studied. (Top) Dominant oscillating frequencies of these events were sorted from low to high (x axis; LFP). (Bottom) Corresponding normalized (to maximum) spike rate during each event of the recorded FS cell (from the same electrode). This cell shows a clear higher spiking rate relationship during higher frequencies.

Large-scale coherence of LFP activities and spikes during wake-sleep γ- and β-oscillations. (A) Field–field correlations: maximum (Max) of the cross-correlation (within a time lag ranging from −50 to 50 ms) averaged over all filtered LFPs (in the γ-frequency range for human and in the β-frequency range for monkey) vs. spatial distance. In both human and monkey, fast oscillations displayed locally correlated dynamics in all states, but the correlations decline with distance. During SWS, correlations stayed high across cortical distances of several millimeters. (B) Spike-field correlations: averaged Rayleigh’s Z value vs. distance from LFP sites for all significantly locked RS and FS neurons. During SWS, FS neurons are phase-locked with a field over up to 3 mm in both human and monkey. This phase-locking disappears during wakefulness. In contrast, RS neurons show less spatial coherence during SWS and no significant correlation with distant LFP sites during wakefulness. (C) Cell–cell correlations: matrices of significant spike synchronization for PMd and MI cells during β-oscillations in monkey. For SWS, the type of target cells is indicated for cells 57/69 with colors (red, FS; and blue, RS). Note that most of the cell–cell interactions over the extent of the array are FS. (D) Spatial distribution of significant cell–cell interactions for two FS cells. Spike synchrony with cell 57/69 can be seen with cells that are spatially far apart. This synchronous spiking could even extend to other cells recorded in another cortical area (from PMd to M1). (E) Example of spike cross-correlogram during SWS and Wake states. Note the presence of a significant peak around zero during SWS that disappears during the Wake state (in green, mean ± 3 SDs of 100 surrogates generated by temporal jittering).

(A) Patterns of strong links (maximum cross-correlation ≥ 0.9 over a delay of ±50 ms) occurring across the grid (human). (B) Patterns of pair-wise LFP spatial correlation for different states. Arrows point to the corresponding spatial profile of strong links at sample times. (C) Size distributions of the coherent patterns. In all states, widespread strong correlation across the grid can be seen, but they are less frequent during the WAKE state and very frequent during SWS. C and D show the percentage and statistical distribution of strong links.

(A) Patterns of strong links (maximum cross-correlation ≥ 0.9 over a delay of ±50 ms) occurring across the grid (Monkey). (B) The spatial correlations are higher during SWS than during the WAKE state. Large patterns of strong links can mostly be seen during SWS. Similar observations can be made for human data (). C and D show the percentage and statistical distribution of strong links.

(A) Wave propagation in the δ-frequency (0.5–4 Hz), γ-frequency (30–50 Hz), and β-frequency (15–30 Hz) ranges during SWS or wakefulness. LFPs in the γ- and β-bands from a single trial are plotted with respect to the spatial arrangement of the recording electrodes. (A1 and A3) Spatiotemporal plots of example LFP waves in human γ (Left) and monkey β (Right) for both SWS (A1) and wakefulness (A3). (A2 and A4) Stereotyped, repetitive spatiotemporal patterns of single oscillations (osci) were frequently observed throughout the recordings. (B) Phase speed distributions across frequency bands and across network states in human. (Left) Plotted are the kernel smoothing density estimates for δ-, β-, and γ-frequency bands during SWS. Speed estimates from individual δ-epochs are plotted on the abscissa (black dots). Propagation in the δ-frequency band exhibited speeds predominantly in the 10–100 mm⋅s⁻¹ range, whereas β- and γ-frequency propagation exhibited higher speeds (Inset; median + median absolute deviation). (Right) γ-Oscillations across different states exhibited similar distributions of propagation speed. Speed estimates from individual γ-epochs in the awake state are plotted on the abscissa (black dots). AWK, awake; Norm., normalized.