Rhythmic oscillations of visual contrast sensitivity synchronized with action

Abstract

It is well known that the motor and the sensory systems structure sensory data collection and cooperate to achieve an efficient integration and exchange of information. Increasing evidence suggests that both motor and sensory functions are regulated by rhythmic processes reflecting alternating states of neuronal excitability, and these may be involved in mediating sensory-motor interactions. Here we show an oscillatory fluctuation in early visual processing time locked with the execution of voluntary action, and, crucially, even for visual stimuli irrelevant to the motor task. Human participants were asked to perform a reaching movement toward a display and judge the orientation of a Gabor patch, near contrast threshold, briefly presented at random times before and during the reaching movement. When the data are temporally aligned to the onset of movement, visual contrast sensitivity oscillates with periodicity within the theta band. Importantly, the oscillations emerge during the motor planning stage, ∼500 ms before movement onset. We suggest that brain oscillatory dynamics may mediate an automatic coupling between early motor planning and early visual processing, possibly instrumental in linking and closing up the visual-motor control loop.

Keywords: action; brain oscillations; phase locking; sensory-motor; vision.

Copyright © 2015 the authors 0270-6474/15/357019-11$15.00/0.

Figures

Figure 1.

Experimental setup and procedure. a, Illustration of the motor and visual tasks. The motor task was reaching and grasping with the right hand a vertical bar close to the right side of the display. Both the participant's right arm and the bar to be grasped were hidden from view by black cardboard (open loop condition). The illustration of the screen shows the background visual noise, the central fixation point, and a left hemifield Gabor stimulus. The white square in the upper left corner of the screen (that was actually hidden from view by the photodiode) was displayed simultaneously to the Gabor (and also to the dynamic visual noise) and recorded by the photodiode to yield the accurate time of stimulus presentation (and of trial onset). b, An example series of snapshots of the visual display. Visual noise and the fixation point were displayed throughout the trial. At a random time from the start of the trial (i.e., from the visual noise and fixation point onset), a Gabor patch was presented for ∼33 ms (two frames) either to the lower right or to the lower left of fixation. The third snapshot shows a right hemifield Gabor as an example. c, Schematic illustration of the timeline of the events during the trial for the self-initiated condition (Experiment 1). The dynamic visual noise and fixation point were displayed for the entire duration of the trial (3 s), as shown by the upper line. The Gabor patch was presented at a random time between ∼0.4 and ∼1.8 s from the start of the trial (middle line). Participants were allowed to initiate the movement at will in a 2 s interval between 0.5 and 2.5 s from the start of the trial. Trials were aborted if movements were executed too early (before 0.5 s from the start of the trial) or too late (after 2.5 s from the start of the trial), as indicated in the third line; trial abortion and successive repetition was signaled by auditory feedback.

Figure 2.

Time courses of visual performance in the orientation discrimination task (in percentage of correct responses) temporally aligned with respect to movement onset (zero time by definition; left column graphs) and relative spectral profiles (right column graphs) are shown for the right (red) and left (blue) hemifield stimuli in the self-initiated movement condition (results for all participants). The nonparametric permutation test yields significant peaks in the theta band (3.5–8 Hz; p < 0.05, Bonferroni corrected for multiple comparisons across the 2–12 Hz frequency range), except for S4 left hemifield (p = 0.06, Bonferroni corrected), compared with the surrogate spectral distributions derived by randomly assigning stimulus presentation times in each individual data set (means and 95% confidence intervals indicated by solid and dashed gray lines, respectively). *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 3.

Time courses of visual performance (in percentage of correct responses) aligned with respect to the visual noise display (i.e., trial onset) are shown for both the right (red) and left (blue) hemifield stimuli in the self-initiated movement condition (left graphs). Individual distributions of movement onset times are plotted at the bottom of each graph (bar histograms). Spectral profiles are reported for the right (red) and left (blue) hemifield stimuli, yielding in both cases no significant differences with respect to the surrogate distributions derived by randomly shuffling stimulus latencies separately for the right and left hemifield data sets (means and 95% confidence intervals indicated by solid and dashed gray lines, respectively; right graphs).

Figure 4.

Visual performance (percentage correct) calculated from the data pooled across subjects (n = 4) and stimulus positions (right and left hemifields) aligned with respect to movement onset (top left graph) and trial onset time (bottom left graph) in the self-initiated movement condition. Spectral analysis is reported in the right column graphs showing a significant peak at 5.6 Hz for the movement-locked performance (p < 0.0001, Bonferroni corrected; top right graph) and no significant oscillatory components for the performance aligned on the start of the trial (bottom right graph). The distribution of movement onset times pooled across subjects and conditions is shown by the bar plot in the bottom left graph. Movements initiated between 1500 and 2500 ms are collapsed in one single bar for illustrative reasons. ****p < 0.0001.

Figure 5.

Individual frequency distributions of the temporal separation between movement onset and Gabor onset in the self-initiated movement condition. Negative values of Gabor-movement onset asynchrony indicate trials in which the Gabor patch was presented before movement onset (black bars), whereas positive asynchrony values indicate trials in which movement was initiated before the Gabor was presented (light gray bars).

Figure 6.

Time course of visual performance (percentage of correct responses) for a subset of near-threshold contrast values aligned to movement onset time (zero time) is shown for the right and left hemifield stimuli in the externally triggered movement condition (top graphs, gray solid lines; results for the two tested subjects). The three colored stars indicate the visual contrast thresholds calculated at three abutting time intervals covering an entire oscillatory cycle. Peaks and troughs in the performance reflect relative low (contrast for the right hemifield stimuli, S4, 7.6 ± 0.35%; S5, 6.9 ± 0.5%, red stars; contrast for the left hemifield stimuli, S4, 7 ± 0.3%; S5, 7.2 ± 0.5%, blue stars; threshold ± SE) and high (contrast for the right hemifield stimuli, S4, 10 ± 0.9%; S5, 8.3 ± 0.67%, black stars; S4, 10.2 ± 0.9%; S5, 8.5 ± 0.9%, gray stars; contrast for the left hemifield stimuli, S4, 9 ± 0.7%; S5, 10.5 ± 1.3%, black stars; S4, 9.08 ± 1%; S5, 10.9 ± 1.6%, gray stars) contrast thresholds. The three corresponding psychometric functions (calculated in the same time intervals shown by the colored stars in the top graphs) indicating the proportion of trials where the Gabor orientation was judged correctly are plotted in the bottom graphs.

Figure 7.

Visual performance (percentage correct) calculated from the data pooled across subjects (n = 2) and stimulus positions (right and left hemifields) aligned with respect to movement onset (top left graph) and sound onset time (bottom left graph) for the externally triggered movement condition. Spectral analysis is reported in the right column graphs showing a marginally significant peak at 4 Hz for the movement-locked performance (p = 0.06, Bonferroni corrected; top right graph) and no significant peaks for the performance aligned on sound presentation time (bottom right graph). The distribution of reaction times pooled across the two tested subjects is shown by the bar plot in the lower row (bottom left graph).