Phase entrainment of human delta oscillations can mediate the effects of expectation on reaction speed

Abstract

The more we anticipate a response to a predictable stimulus, the faster we react. This empirical observation has been confirmed and quantified by many investigators suggesting that the processing of behaviorally relevant stimuli is facilitated by probability-based confidence of anticipation. However, the exact neural mechanisms underlying this phenomenon are largely unknown. Here we show that performance changes related to different levels of expectancy originate in dynamic modulation of delta oscillation phase. Our results obtained in rhythmic auditory target detection tasks indicated significant entrainment of the EEG delta rhythm to the onset of the target tones with increasing phase synchronization at higher levels of predictability. Reaction times correlated with the phase of the delta band oscillation at target onset. The fastest reactions occurred during the delta phase that most commonly coincided with the target event in the high expectancy conditions. These results suggest that low-frequency oscillations play a functional role in human anticipatory mechanisms, presumably by modulating synchronized rhythmic fluctuations in the excitability of large neuronal populations and by facilitating efficient task-related neuronal communication among brain areas responsible for sensory processing and response execution.

Figure 1.

Reaction time correlates with the level of expectancy. A, Auditory target detection paradigm of experiment 1. Four different cue tones (black) predicted the target tone (gray) to be the next stimulus with increasing probability paralleling the increase of cue-tone frequencies (p = 0.1, p = 0.37, p = 0.64 and p = 0.91). Participants were to press a response key to the target tone. B, Reaction times (RT) significantly decreased with increasing predictability of the target (n = 13; ANOVA, p < 10⁻⁹, with Tukey's post hoc tests, p < 0.01). Error bars indicate SEM. C, In experiment 2, two different cue tones predicted the timing of the target tone with different probabilities. An early target (1350 ms after the cue) was delivered with p = 0.2 after cue 1 and with p = 0.8 after cue 2. On trials with no early target, a late target (2700 ms after the cue) was delivered (p = 0.8 after cue 1 and p = 0.2 after cue 2). D, The early-target RT was significantly shorter after cue 2 (p = 0.8 probability, third bar) than after cue 1 (p = 0.2 probability, first bar) (p < 0.01, Tukey's post hoc test). In the absence of an early target, delivery of the late target could be predicted with 100% certainty, resulting in faster RTs compared with the early target with p = 0.2 (following cue 1, p < 0.05 and cue 2, p = 0.08). C1, cue 1; C2, cue2; E, early target; L, late target. *p < 0.05; **p < 0.01.

Figure 2.

Phase entrainment of the cortical delta oscillation. A–D, Distributions of delta phase values (measured at Cz) at target onset are presented on rose diagrams with the radial extent of the circle segments representing the probability of the given phase range. Trials with 10% (A), 37% (B), 64% (C), and 91% (D) target probabilities were separately pooled from all (n = 13) participants. E–H, Individual (gray) and average (black) phase histograms for the four different target probabilities (two cycles; idealized delta waves in red in E, negativity is upward). Unimodal phase preference of the distributions is clearly visible, with the mean phases near the negative peak of the delta waves (from 10% to 91%, in radians: 2.56, 2.85, 3.10, −3.03). The accuracy of phase entrainment (measured as the concentration (sharpness, κ) of phase histograms) increased with increasing levels of target predictability (κ values from 10% to 91%: 0.74, 0.82, 1.07, 1.19). The difference between the 37% and 64% as well as between the 64% and 91% conditions was significant (permutation tests with p values for the comparisons of 10% vs 37%, 37% vs 64% and 64% vs 91%: 0.094, 0.0001, 0.036, respectively). I, J, Distribution of delta-phase values (measured at Cz) at the time of the expected delivery of the early target in experiment 2. Trials from late-target trials (i.e., no early target was delivered) were pooled separately for p = 0.2 (I) and p = 0.8 (J) early-target probability from all participants (n = 11). K, L, Individual (gray) and average (black) phase histograms for p = 0.2 (K) and p = 0.8 (L) target probabilities. Phase values were significantly more concentrated for high- than for low-probability targets (p = 0.024, permutation test; κ (mean phase): 0.27 (−2.84) and 0.40 (−3.04), for the 20% and 80% target probabilities, respectively). M, Average EEG traces from experiment 1 aligned at target onset (0 ms), filtered between 0.5–3 Hz (top) and 0.5–20 Hz (bottom). The traces were averaged separately for the four different levels of target predictability (blue, 10%; orange, 37%; green, 64%; purple, 91%). Note the amplitude increase at target onset with increasing levels of target predictability. N, Average filtered EEG traces from experiment 2 aligned at the presentation of the cue tone, shown separately for the two different cue tones (late-target trials, only), filtered between 0.5–3 Hz (top) and 0.5–20 Hz (bottom). The average delta-wave amplitude was markedly higher at 1350 ms postcue (the expected onset of the early target marked by the vertical dotted line) for cue 2 (early target by p = 0.8; red line) than for cue 1 trials (p = 0.2; blue).

Figure 3.

Phase-entrainment of delta-band EEG oscillations. A–D, ERP images of single-trial responses filtered between 0.5 and 3 Hz from experiment 1, sorted by phase-values from −π to π at target onset time. Trials from all 13 subjects at Cz site from 10%, 37%, 64% and 91% probability conditions are shown in plots A–D, respectively. x-axis: time in ms, y-axis: individual EEG traces, colors represent amplitude values. Shaded areas mark the random interval where the cues were presented between −1500 and −1200 ms preceding the target. Data were smoothed using a vertical window of 20 trials. Vertical white line at 0 ms represent the onset of the target tone, curved vertical black lines show single reaction time values, gray lines show SEM. Area between horizontal dashed lines contains trials with positive amplitude at target onset. Note the reduction of trials falling into this region with increasing target probability and the presence of oscillatory activity during the whole epochs. E, F, ERP images of single-trial responses from experiment 2 from all 11 subjects, similar to plots A–D. Epochs from late-target trials, when no early target was delivered, are sorted by delta-phase values at the early (1350 ms) expected onset time (marked by vertical white lines); cue (0 ms) and late target (2700 ms) onset times are indicated by vertical black lines. Twenty percent and 80% expectancy conditions at Position 1 are shown in E and F, respectively. The proportionally smaller number of trials with less favorable phase values (between the horizontal dashed lines) in the 80% condition demonstrates that the accuracy of delta-phase entrainment increased at higher target probability.

Figure 4.

Task performance is correlated with delta phase modulation. First row, Central (Cz) delta-phase values measured at target onset, pooled and sorted in ascending order from all trials of all participants in experiment 1 (1300 trials), separately for the four levels of target probability (from the left: 10%, 37%, 64%, 91%). The nonlinearity of the curves is the consequence of phase entrainment. Second row, RTs arranged in the same way. Data were smoothed for visualization using a 100-point sliding window (gray lines, SEM resulting from the smoothing). RTs significantly correlated with the delta phase at target onset (circular-linear correlation coefficients and p values are indicated on the plots). Fastest reactions were observed when the delta phase at the target onset fell on the rising slope of delta oscillation, near the negative peak (delta phase in radians at the minimal reaction time, from 10% to 91%: −2.76, −2.68, −2.56, −1.98, respectively). Third and forth rows, Latency and amplitude of the delta-peak component arranged similarly as in the rows above. These measures also correlated with the delta phase at the target onset, with minimal latency and maximal amplitude near the negative peak of delta oscillation (delta phase at the minimal latency, from 10% to 91%: −2.71, −2.57, −2.14, −2.13, respectively; delta phase at maximal amplitude, from 10% to 91%: −3.12, −3.11, −2.96, −2.93, respectively).