Dynamic large-scale network synchronization from perception to action

Abstract

Sensory-guided actions entail the processing of sensory information, generation of perceptual decisions, and the generation of appropriate actions. Neuronal activity underlying these processes is distributed into sensory, fronto-parietal, and motor brain areas, respectively. How the neuronal processing is coordinated across these brain areas to support functions from perception to action remains unknown. We investigated whether phase synchronization in large-scale networks coordinate these processes. We recorded human cortical activity with magnetoencephalography (MEG) during a task in which weak somatosensory stimuli remained unperceived or were perceived. We then assessed dynamic evolution of phase synchronization in large-scale networks from source-reconstructed MEG data by using advanced analysis approaches combined with graph theory. Here we show that perceiving and reporting of weak somatosensory stimuli is correlated with sustained strengthening of large-scale synchrony concurrently in delta/theta (3-7 Hz) and gamma (40-60 Hz) frequency bands. In a data-driven network localization, we found this synchronization to dynamically connect the task-relevant, that is, the fronto-parietal, sensory, and motor systems. The strength and temporal pattern of interareal synchronization were also correlated with the response times. These data thus show that key brain areas underlying perception, decision-making, and actions are transiently connected by large-scale dynamic phase synchronization in the delta/theta and gamma bands.

Keywords: Action; Communication; MEG; Perception; Somatosensory; Synchronization.

Figure 1.. A schematic overview of the analysis pipeline. This figure shows the different analysis steps and outputs of the results (for a–m, see Methods).

Figure 2.. Task and behavioral performance. (A) Schematic illustration of the experimental para digm with a stream of constant-intensity somatosensory stimuli presented at 1.5- to 4.5-s intervals and the corresponding behavioral Hit-Miss time series for a representative subject. Blue bars denote consciously perceived stimuli, and the red bars denote unperceived stimuli. (B) Individual (black lines) and group (red line) response time (RT) distributions.

Figure 3.. Large-scale delta- and gamma-band synchronization characterizes neuronal processing of perceived but not unperceived stimuli. (A) Time-frequency representations of the extent of significant interareal synchronization as estimated with PLV for perceived (Hit) stimuli, unperceived (Miss), as well as for their difference (Hit-Miss) compared with the prestimulus baseline (N = 12) (Wilcoxon signed-ranked test, p < 0.05, corrected for multiple comparisons). Sustained gamma-band (40–60 Hz) synchronization and delta/theta- (δ/θ, 3–7 Hz) band synchronization were stronger for Hits than Misses. The color indicates the connection densities of positive (K+) and negative (K−) observations, that is, the fractions of connections with a statistically significant positive or negative difference from the baseline level, respectively. (B) Time-frequency representations of the extent of significant interareal synchronization as estimated with iPLV.

Figure 4.. Gamma- and delta/theta-band synchronization is not artificial and predicts the speed of sensorimotor decisions. (A) The mean coupling strength () for the significant edges for Hits in the original (red line) and surrogate data (blue line) in delta/theta- (δ/θ) and gamma- (γ) frequency bands. (B) Connection density (K) as a function of time for the difference between Hits and Misses separately for trials with fast (red) and slow (blue) RTs. Vertical lines show the mean RT in these two categories: 356 ± 122 ms (mean ± SD across subjects) for the trials with fast RTs and 594 ± 229 ms for the trials with slow RTs. The horizontal bars above the plots show the time window in significant difference between trials with fast and slow trial RTs (Wilcoxon signed-ranked test, p < 0.05, corrected for multiple comparisons). The trials were split at the median RT of each subject and the mean of these median RTs was 464 ± 142 ms (mean ± SD across subjects).

Figure 5.. Large-scale synchronization connects somatosensory and attentional brain systems. (A) Graph of the significant differences in the strength of interareal phase synchrony as estimated with PLV between Hits and Misses in the delta/theta-frequency band (δ/θ, 3–7 Hz) and in the time window of 125–275 ms from stimulus onset (cf. Figure 2C). Lines connect the coupled parcels and line colors are determined by the parcel brain systems (see below). Delta/theta-band synchronization was centered on the contralateral (left hemispheric) sensorimotor (SM, red) system, and in particular, on the primary somatosensory cortex (SI) therein that was strongly and bilaterally coupled with frontal and parietal regions. (B) Graph of gamma-band synchronization (γ, 40–60 Hz) reveal significantly stronger connections for Hits than Misses over 225–375 ms from stimulus onset. Stronger gamma-band synchronization for Hits than Misses was observed within SM and between SM and the ipsilateral frontoparietal and dorsal (FP and DA, blue and purple) attention networks. Graphs are displayed on an inflated and flattened cortical surface with 300 (A) and 200 (B) of the most central edges based on parcel PageRank centralities selected for visualization. SI is primary and SII is secondary somatosensory area. MI and SMA are primary and supplementary motor areas, respectively. Parcel and corresponding node colors indicate the Yeo-atlas brain systems derived from BOLD intrinsic connectivity connectome. SM = somatomotor (SM), green = visual (Vis), yellow = ventral attention network (VAN), purple = dorsal attention network (DAN), white = limbic (Lim), gray = default mode network (DMN).

Figure 6.. Time-varying subsystem connectivity within and between attentional systems and SM. (A) Connection densities of significant interareal gamma-band (40–60) Hz and delta/theta-band (3–7 Hz) synchronization among Yeo-atlas brain systems for Hits and Misses compared with baseline and for their difference. Only such system-system connections are shown that exhibit greater connection densities than expected by chance in shuffled graphs (p < 0.05, permutation statistics, see Methods). The color, line width, and radius of circles of the system-system connections indicates the connection density of significant couplings (K_systems) within (circles) or between (lines) the functional systems in a time window of 225–375 ms. (B) Time-resolved cumulative connection densities (K) of gamma- and delta/theta-band synchronization estimated separately for within-attentional (DAN, FNP, and VAN), between SM and attentional, and all other functional subsystems. Synchronization in task-positive sensory and attentional systems predicted subsequent conscious perception in gamma band, whereas synchronization in the delta/theta band was observed in SM along with connections to and within-attentional systems throughout the time course of stimulus detection.

Figure 7.. Synchrony within and between attentional and sensorimotor systems is frequently observed in individual subject’s statistical analyses. (A) All significant connections among functional subsystems separately for each subject. Significant connections are shown with gray tone that is scaled relative to the connection density between (lines) or within (circles) the subsystems. Red surroundings indicate the most common within-subsystem connections across the subjects. (B) All significant connections across all subjects in individual subject statistical analyses. Line color indicates the number of subjects (N) in which significant connections were were observed.