Coordinated within-trial dynamics of low-frequency neural rhythms controls evidence accumulation

Abstract

Higher cognitive functions, such as human perceptual decision making, require information processing and transmission across wide-spread cortical networks. Temporally synchronized neural firing patterns are advantageous for efficiently representing and transmitting information within and between assemblies. Computational, empirical, and conceptual considerations all lead to the expectation that the informational redundancy of neural firing rates is positively related to their synchronization. Recent theorizing and initial evidence also suggest that the coding of stimulus characteristics and their integration with behavioral goal states require neural interactions across a hierarchy of timescales. However, most studies thus have focused on neural activity in a single frequency range or on a restricted set of brain regions. Here we provide evidence for cooperative spatiotemporal dynamics of slow and fast EEG signals during perceptual decision making at the single-trial level. Participants performed three masked two-choice decision tasks, one each with numerical, verbal, or figural content. Decrements in posterior α power (8-14 Hz) were paralleled by increments in high-frequency (>30 Hz) signal entropy in trials demanding active sensory processing. Simultaneously, frontocentral θ power (4-7 Hz) increased, indicating evidence integration. The coordinated α/θ dynamics were tightly linked to decision speed and remarkably similar across tasks, suggesting a domain-general mechanism. In sum, we demonstrate an inverse association between decision-related changes in widespread low-frequency power and local high-frequency entropy. The cooperation among mechanisms captured by these changes enhances the informational density of neural response patterns and qualifies as a neural coding system in the service of perceptual decision making.

Keywords: EEG; decision making; entropy; neural oscillations; single-trial analyses; synchronization.

Figure 1.

Schematic illustration of trial design (A), as well as the stimuli and conditions implemented in the numerical, verbal, and figural choice reaction tasks (B).

Figure 2.

Summary of results for single-trial correlation analyses, separately for each CRT (columns from left to right: numerical, verbal, and figural task). The color-coded images represent electrode (y-axis) time regions (x-axis) with reliable associations (group level analysis; masked at p < 0.05, cluster level) between oscillatory power in the α (top row) or θ frequency (middle row) range and single-trial RT distributions (RT histograms, bottom row). Vertical black dotted line indicates stimulus onset; red dotted line indicates the median RT across trials and participants. For each color image, the electrodes are approximately ordered from anterior (top) to posterior (bottom) locations. The color scale represents t values. Warm colors represent a positive association (i.e., higher power associated with shorter RT); cold colors represent a negative relationship (i.e., higher power associated with longer RT).

Figure 3.

Topographical distribution of reliable single-trial power–RT associations for each CRT (rows from top to bottom: numerical, verbal, and figural task) within the α (two left-most columns) and θ frequency ranges (two right-most columns). The topographical maps represent mean t values averaged across two representative time windows (early: 0.3–0.5 s; late: 0.6–0 1 s poststimulus). Only reliable electrode time points (group level analysis; masked at p < 0.05, cluster level) were included in the averages within the respective time window. Warm colors represent a positive association (i.e., higher power associated with shorter RT); cold colors represent a negative relationship (i.e., higher power associated with longer RT). The small black dots indicate the central (FC1, FCz, FC2, C1, Cz, C2) and posterior (P7, P5, P3, Pz, P2, P4, P8, PO7, PO3, POz, PO4, PO8, O1, Oz, O₂) electrode regions of interest used for further analyses of signal power changes in the α and θ frequency range.

Figure 4.

Summary of single-trial dynamics of signal power changes at selected representative electrode clusters (see Fig. 3), separately for the numerical (top row), verbal (middle row), and figural task (bottom row) in the α (the two left-most columns) and θ frequency range (the two right-most columns). The y-axis for each plot represents the individual trials sorted according to RT from top to bottom. The S-shaped solid white line indicates the respective RT for each trial. The dotted white line indicates stimulus onset. The color scale represents the relative change in signal power with regard to a prestimulus baseline (see Materials and Methods). Each plot represents data from 6642 trials for the numerical, 5959 trials for the verbal, and 6780 trials for the figural task. For visualization, the images were smoothed with a 100 trial-wide boxcar function from top to bottom after sorting. In these plots, each horizontal row represents one single trial. By comparing the same row (i.e., trial) from left to right within a given task condition, the dynamics of the same trial across regions and frequency ranges is revealed.

Figure 5.

Time-varying changes in signal amplitude for stimulus-present (STIM, dark gray lines) and stimulus-absent (NOSTIM, black lines) conditions. The grand-average relative changes in signal amplitude (y-axis) for central and posterior electrode regions of interest (for details, see Fig. 3) are plotted separately for each task (rows from top to bottom: numerical, verbal, figural) in the α (the two left-most columns) and θ frequency range (the two right-most columns). The gray shaded patches represent time windows for which the cluster-based permutation tests revealed reliable differences (group level analysis; p < 0.05, cluster level) between STIM and NOSTIM conditions. The x-axis represents time (in seconds) relative to stimulus onset.

Figure 6.

Time-varying changes in signal entropy (>30 Hz) for the stimulus-present condition. Each row presents the results for a given task (from top to bottom: numerical, verbal, figural). The time evolution of changes in entropy, expressed in z-values (y-axis), is shown on the left for a central (black line) and a posterior (red line) electrode region of interest. The shaded black/red patches surrounding the thick lines represent ±2 SE. The light gray shaded patches in the back represent time windows for which the cluster-based permutation tests revealed reliable changes in signal entropy compared with baseline (group level analysis; p < 0.05, cluster level). The significant time windows for the central region of interest were long-lasting and only in the negative direction, for the posterior region comparably short-lasting and exclusively in the positive direction. The x-axis represents time (in seconds) relative to stimulus onset. The topographical distribution of stimulus-locked changes in signal entropy is illustrated for two representative time windows (early: 0.1–0.4 s; late: 0.5–0.9 s poststimulus) in the middle and right-most column. Small black dots indicate the central (FC1, FCz, FC2, C1, Cz, C2) and posterior (PO7, PO3, POz, PO4, PO8, O1, Oz, O₂) electrode regions of interest used for analyses. The early posterior increase and the later decrease over central regions are clearly visible.

Figure 7.

Single-trial dynamics of entropy changes illustrated for selected electrode regions of interest (for details on electrode selection, see Fig. 6). The left column represents single-trial entropy changes (expressed in z-values) over central recording locations for the numerical (top row), verbal (middle row), and figural task (bottom row). The same information for posterior electrode sites is illustrated in the right column. The y-axis for each plot represents the individual trials sorted according to RT from top to bottom. The S-shaped solid white line indicates the respective RT for each trial. The dotted white line indicates stimulus onset. The color scale indicates the relative change in high-frequency signal entropy with regard to a prestimulus baseline expressed in z-values (see Materials and Methods). Each plot represents data from 6642 trials for the numerical, 5959 trials for the verbal, and 6780 trials for the figural task. For visualization, the images were smoothed with a 100 trial-wide boxcar function from top to bottom after sorting. Each horizontal row represents one single trial. The decrease in entropy over central regions is maximal around the RT and varies with it (i.e., slightly S-shaped). By contrast, the initial increase in entropy over posterior recording sites is related to stimulus onset (i.e., rather parallel to the dashed white line indicating stimulus onset).

Figure 8.

Direct comparison of poststimulus changes in signal power (red) and high-frequency signal entropy (dark gray). The solid lines in each plot indicate the group average of each measure, whereas the surrounding red/gray shaded patches represent ±2 SE. The y-axis on the left (gray) represents changes in entropy with regard to a prestimulus baseline expressed in z-scores. The y-axis on the right represents the percentage change in signal power from baseline for posterior α (left column) and central θ (right column) activity. For the posterior electrode cluster, it becomes apparent that the peak in entropy increases follows the early stimulus-related peak in α power changes and is co-occurring with the initial half of the α desynchronization that follows. By contrast, for central recording locations, both the increase in θ activity as well as the decrease in high-frequency power reach their maximum or minimum, respectively, around the mean RT and slowly return to baseline levels thereafter.