The Common Rhythm of Action and Perception

Abstract

Research in the last decade has undermined the idea of perception as a continuous process, providing strong empirical support for its rhythmic modulation. More recently, it has been revealed that the ongoing motor processes influence the rhythmic sampling of sensory information. In this review, we will focus on a growing body of evidence suggesting that oscillation-based mechanisms may structure the dynamic interplay between the motor and sensory system and provide a unified temporal frame for their effective coordination. We will describe neurophysiological data, primarily collected in animals, showing phase-locking of neuronal oscillations to the onset of (eye) movements. These data are complemented by novel evidence in humans, which demonstrate the behavioral relevance of these oscillatory modulations and their domain-general nature. Finally, we will discuss the possible implications of these modulations for action-perception coupling mechanisms.

Figure 1

Schematic representation of the neuronal oscillatory modulations underlying the movement-locked fluctuations in visual performance and the main behavioral paradigm used to investigate this phenomenon. The colored lines show a cartoon of the ongoing delta/theta-band oscillatory activity during the pre-movement epoch in example trials. Movement onset (black arrow) occurs at a systematic phase (in this example the trough) of the ongoing rhythmic activity, revealing oscillatory phase-alignment to the (future) movement onset (see Tomassini et al., 2017). Alternatively, movement-locking of delta/theta phases may be due to phase-resetting by an endogenous, movement-related, signal (e.g. corollary discharge) which is generated during motor preparation at a systematic moment in time before movement onset (grey shaded area). In each trial, a visual probe (colored dot) is presented at a random time (hence, at a random phase) both before and after movement onset. Movement-locked temporal averaging of the visual performance for the presented probes yields an oscillatory pattern (grey line; see Tomassini et al., 2015, 2017; Benedetto et al., 2016, 2017), reflecting 1) the influence of the ongoing phase on visual performance and 2) the consistent alignment of the ongoing phase to movement onset.

Figure 2

Box on top, experimental procedure from Benedetto and Morrone, 2017. Participants performed saccades at their own pace to stationary saccadic targets (fixation 1 and fixation 2). At random delays from the saccadic onset (Δt), a brief Gabor stimulus with a contrast increment in its upper or lower side was presented and participants reported the location of the increment. Box on bottom: left panel, Pre-saccadic and post-saccadic contrast discrimination performance as a function of time from saccadic onset. The gray area represents ±1 SEM from bootstrapping; thick lines represent the best sinusoidal fit to the data for pre-saccadic responses (red, ~ 3 Hz) and for post-saccadic responses (green, ~2 Hz). Blue dots indicate the moment of maximal visual suppression caused by the execution of the saccade (saccadic suppression). Dashed vertical and horizontal lines indicate saccadic onset (time zero) and the median probability of correct response, respectively. Right panel, FFT mean amplitude spectra ±1 SEM for pre-saccadic responses (red) and post-saccadic responses (green), showing a significant peak at around 3 and 2 Hz, respectively. Asterisks indicate significance (0.05 > * > 0.01).

Figure 3

Box on top-left, timeline of the trial from Tomassini et al., 2017. A visual cue (change in color of the fixation cross) is shown after a variable delay from the start of the trial and indicates whether participants have to wait for a short (1.5 s) or a long (2.3 s) time interval before executing the hand movement (isometric contraction). The visual cue offset marks the start of the time interval that participants have to wait before executing the movement. Bar histograms show the distribution of movement onset times for the short (pink) and long (blue) time intervals. The dashed vertical lines indicate the mean onset times (short: 1.5 ± 0.2 s; long: 2.22 ± 0.24 s; mean ± s.d.). At random times between –0.35 and +0.25 s relative to the instructed movement time, a near-threshold contrast Gabor tilted 45 deg clockwise or counterclockwise is briefly flashed for 16 ms. Box on top-right, predictive value of the phase of sinusoidal (basis) functions for perceptual performance (time-locked to movement onset). The gray-shaded area represents the jackknife standard error. The black horizontal bars indicate the significant frequencies (p<0.05). Box on bottom: left, predictive value of the 4 Hz theta (neuronal) phase for perception as a function of the time where the phase was estimated relative to movement onset. The gray-shaded area represents the jackknife standard error. Center, time course of theta phase-locking to movement onset (estimated by means of a measure of phase reliability; for details see Tomassini et al., 2017). The gray-shaded area represents the standard error of the mean. The black horizontal bars indicate significant time points. Right, topography of the predictive value of theta phase for perception at −1.4 s and at -0.1 s. Significant channels are marked by bigger black circles.

Figure 4

Box on top: left, time course of the Point of Subjective Simultaneity (PSS± 1 SEM) for audio-visual stimuli, expressed as a function of movement onset (from Benedetto et al., 2018). The red line shows the best sinusoidal fit (frequency =8.2 Hz). Right, spectral components in the time course of PSS that show phase-consistency across subjects (see Benedetto et al., 2018 for methods details). The horizontal thick line indicates the significant frequencies (p < 0.05). Box on bottom: left, schematic of the experimental procedure from Tomassini et al., 2018. Four auditory tones were played at 1 Hz. Participants were asked to continue the sequence of tones by pressing a button four times with their right index finger at the same rate as the sound presentation. At random times between the 3rd and the 4th button press (marked in green), two visual flashes (5 ms each) were presented separated by a variable temporal interval (probe). Participants reported whether the probe interval was shorter or longer compared with the standard interval (150 ms, presented at the beginning of each block; not shown). Center, time courses in perceived duration aligned to the 4th tap and best-fitting Gaussian functions for trials in which participants tapped at a faster rate, yielding short inter-tap intervals (yellow) and at a slower rate, yielding long inter-tap intervals (dark green). Right, the mean of the best-fitting Gaussian function (indexing the latency of maximal perceived time expansion) is plotted against half of the inter-tap interval for short (yellow), accurate (light green), and long (dark green) trials. The diagonal indicates that maximal perceived time expansion occurs halfway between the two consecutive finger taps.