Decision-related perturbations of decision-irrelevant eye movements

Abstract

It is well established that ongoing cognitive functions affect the trajectories of limb movements mediated by corticospinal circuits, suggesting an interaction between cognition and motor action. Although there are also many demonstrations that decision formation is reflected in the ongoing neural activity in oculomotor brain circuits, it is not known whether the decision-related activity in those oculomotor structures interacts with eye movements that are decision irrelevant. Here we tested for an interaction between decisions and instructed saccades unrelated to the perceptual decision. Observers performed a direction-discrimination decision-making task, but made decision-irrelevant saccades before registering their motion decision with a button press. Probing the oculomotor circuits with these decision-irrelevant saccades during decision making revealed that saccade reaction times and peak velocities were influenced in proportion to motion strength, and depended on the directional congruence between decisions about visual motion and decision-irrelevant saccades. These interactions disappeared when observers passively viewed the motion stimulus but still made the same instructed saccades, and when manual reaction times were measured instead of saccade reaction times, confirming that these interactions result from decision formation as opposed to visual stimulation, and are specific to the oculomotor system. Our results demonstrate that oculomotor function can be affected by decision formation, even when decisions are communicated without eye movements, and that this interaction has a directionally specific component. These results not only imply a continuous and interactive mixture of motor and decision signals in oculomotor structures, but also suggest nonmotor recruitment of oculomotor machinery in decision making.

Keywords: decision making; eye movement; visual motion.

Fig. 1.

Procedure. On a given trial, random-dot motion stimuli were displayed after observers fixated stably for 1 s. At motion offset, a saccade target appeared to either the left or right side of the visual field. Observers made a saccadic eye movement to the target as quickly as possible. After the saccade, they were instructed to report the motion direction with a button press. The contrast polarity of dots and the background in the figure is reversed for illustrative purpose only. The dashed lines depicting the aperture were not shown in the experiments. An example trial from Exp. 1 is shown here.

Fig. 2.

Psychometric functions and saccade metrics in Exps. 1 and 2. (A) The psychometric functions for congruent vs. incongruent conditions, depicted by red and blue lines, respectively. The error bars on the data points reflect SEM across observers, and the horizontal error bars on the 75% accuracy threshold indicate bootstrapped 68% confidence intervals (CIs). (B and C) Saccade reaction times (B) and saccade peak velocities (C) as a function of motion coherence in Exp. 1. (B) Color-scaled data represent viewing duration in the congruent and the incongruent condition (red vs. blue: 100 ms, orange vs. light blue: 200 ms, and yellow vs. cyan: 400 ms). (C) Red and blue indicate saccade peak velocities in the congruent and incongruent conditions, respectively. Solid and dashed lines are the best-fitting lines for the congruent and incongruent conditions, respectively. Error bars are bootstrapped 95% CIs. (D and E) Saccade reaction times (D) and saccade peak velocities (E) as a function of motion coherence in Exp. 2.

Fig. S1.

Individual psychometric functions for the motion-direction discrimination task in Exp. 1. Red and blue lines indicate psychometric function for the congruent and incongruent condition, respectively. Horizontal error bars represent bootstrapped 68% CIs on the 75% accuracy threshold. This suggests that the main finding of Exp. 1 did not result from the different task performance between the congruent and incongruent conditions.

Fig. S2.

Psychometric functions in Exp. 1 for the congruent (Left) and incongruent (Right) conditions, respectively. Color-scaled data represent viewing duration in the congruent and incongruent conditions (red vs. blue: 100 ms; orange vs. light blue: 200 ms; and yellow vs. cyan: 400 ms).

Fig. S3.

Saccade amplitude as a function of motion coherence. (A) Saccade amplitude in Exp. 1. Color-scaled data represent viewing duration in the congruent and incongruent conditions (red vs. blue: 100 ms; orange vs. light blue: 200 ms; and yellow vs. cyan: 400 ms). Saccade amplitude did not increase as motion coherence increased in both the congruent [F(4, 16) = 1.749, P = 0.19] and incongruent conditions [F(4, 16) = 2.217, P = 0.11]. (B) Saccade amplitude in Exp. 3. Red, orange, and yellow lines represent saccade amplitude for 100, 200, and 400 ms viewing duration, respectively. All of the lines are best-fitting lines to the data.

Fig. 3.

Comparison of saccade reaction time benefits between Exps. 1 and 2. Saccade reaction time benefit was calculated by subtracting saccade reaction times for the congruent condition from saccade reaction times for the incongruent condition. Red and blue lines represent saccade reaction time benefit in Exps. 1 and 2, respectively. Error bars are bootstrapped 95% CIs.

Fig. S4.

Individual psychometric functions for the motion-direction discrimination task in Exp. 3. Each observer reported motion direction after making a saccadic eye movement by pressing a designated keyboard button. All observers’ psychometric functions indicate that the difficulty of the task was modulated by the motion coherence. Horizontal error bars represent bootstrapped 68% CIs on the 75% accuracy threshold.

Fig. 4.

Saccade metrics in Exps. 3 and 4. (A) Saccade reaction times in Exp. 3 are plotted as a function of motion coherence for each viewing duration (red: 100 ms; orange: 200 ms; and yellow: 400 ms), averaged across motion direction (up and down). (B) Saccade peak velocities in Exp. 3 are plotted as a function of motion coherence for each viewing duration (red: 100 ms; orange: 200 ms; and yellow: 400 ms), averaged across motion direction (up and down). (C) Manual reaction times in Exp. 4 are plotted as a function of motion coherence for each viewing duration (orange: 200 ms; yellow: 400 ms), averaged across motion direction (up and down). Best-fitting lines are shown. Error bars are bootstrapped 95% CIs.

Fig. S5.

Psychometric functions in Exp. 3 (blue) and Exp. 4 (red). The horizontal error bars represent 68% CIs around 75% accuracy threshold from 1,000 bootstrapped fits. In Exp. 3, threshold is 15.27% and CI = (14.48, 15.52), and in Exp. 4, threshold is 16.25% and CI = (15, 16.89). These results suggest that the different results in Exps. 3 and 4 were not caused by different behavioral performance on motion-direction discrimination tasks in each experiment.