The influence of stimulus and behavioral histories on predictive control of smooth pursuit eye movements

Abstract

The smooth pursuit system has the ability to perform predictive feedforward control of eye movements. This study attempted to examine how stimulus and behavioral histories of past trials affect the control of predictive pursuit of target motion with randomized velocities. We used sequential ramp stimuli where the rightward velocity was fixed at 16 deg/s while the leftward velocity was either fixed (predictable) at one of seven velocities (4, 8, 12, 16, 20, 24, or 28 deg/s) or randomized (unpredictable). As a result, predictive pursuit responses were observed not only in the predictable condition but also in the unpredictable condition. Linear mixed-effects (LME) models showed that both stimulus and behavioral histories of the previous two or three trials influenced the predictive pursuit responses in the unpredictable condition. Intriguingly, the goodness of fit of the LME model was improved when both historical effects were fitted simultaneously rather than when each type of historical data was fitted alone. Our results suggest that predictive pursuit systems allow us to track randomized target motion using weighted averaging of the information of target velocity (stimulus) and motor output (behavior) in past time sequences.

Figure 1

(A) Examples of eye position traces (colored lines) from a representative observer in the predictable condition where the rightward velocity was fixed at 16 deg/s while the leftward velocity was fixed at one of seven velocities (4, 8, 12, 16, 20, 24, or 28 deg/s). One trial consisted of a sequence of the rightward and leftward ramp motion, and each panel shows a typical example of two consecutive trials. There was no pause between ramps, and the starting position was always the same for the initial rightward ramp. Gray lines represent the target position. B: Averaged traces of eye velocity from a representative observer in the predictable condition. The colors of each eye velocity trace correspond to the seven target velocities (same as in Fig. 1A), and gray lines represent target velocities. The time of 0 ms represents the timing of target reversal. C: Examples of eye position (upper panel) and velocity (lower panel) transition from a representative observer in the unpredictable condition where the leftward velocity was randomized within the seven velocities. The figure includes a typical example of five consecutive trials. Black lines represent the eye position and velocity whereas gray lines represent target motion. In all the panels, upward deflections show rightward eye motion.

Figure 2

Eye velocity in a representative trial when the target speed was 16 deg/s. The top panel shows the eye velocity after filtering (30 Hz low-pass filter, light red line), the eye velocity with moving average applied to it (40-ms window, dark red line), and the target velocity (gray solid line). The threshold to detect the onset of predictive pursuit is represented by a gray dotted line. The bottom panel shows eye acceleration in the same trial. The yellow shaded region represents the time that the mean eye deceleration was calculated (i.e., the time between the eye deceleration onset and timing of eye reversal). The time of 0 ms represents the timing of target reversal. Upward deflections show rightward eye motion.

Figure 3

Predictive pursuit responses for the predictable condition (left panels) and unpredictable condition (right panels). (A,B) Eye deceleration onset relative to the target reversal as a function of target velocity. (C,D) Timing of eye reversal relative to the target reversal as a function of target velocity. (E,F) Mean eye deceleration as a function of target velocity. The gray circles and lines represent the values of each observer and black circles and lines represent the mean values of all the observers. Error bars indicate 1 SEM.

Figure 4

Effects of behavioral history on the timing of eye reversal in the predictable condition. The timing of eye reversal was ranked in ascending order at each target velocity, with the top 20% classified as “UPPER” and the bottom 20% classified as “LOWER”. Then, trials were sorted based on the classification of the n-1 (A) or n-2 trial (B). The left node shows the mean timing of eye reversal sorted by the classification, and the right node shows the mean of both trials. In the left node, the open symbols and solid lines represent the trials preceded by a response from the UPPER trials, and the filled symbols and dashed lines represent the trials preceded by a response from the LOWER trials. The color of symbols and lines correspond to the seven target velocities (same as in Fig. 1A). Error bars indicate 1 SEM.

Figure 5

Effects of stimulus and behavioral histories on the timing of eye reversal in the unpredictable condition. For the stimulus history, trials were sorted based on whether the target velocity in the n-1 (A) or n-2 trial (B) was 4 deg/s (red) or 28 deg/s (blue). For the behavioral history, trials were sorted by the same classification as the predictable condition (C: trials sorted by the n-1 trial; D: trials sorted by the n-2 trial). In the left node, the open symbol and solid line represent the trials preceded by a response from the UPPER trials, and the filled symbols and dushed lines represent the trials preceded by a response from the LOWER trials. Error bars indicate 1 SEM.

Figure 6

Pooled distribution of the normalized timing of eye reversal across all observers (bin size, 0.25). The values of median of each distribution are below; (4 deg/s: 1.00; 8 deg/s: 0.71; 12 deg/s: 0.39; 16 deg/s: 0.06; 20 deg/s: -0.08; 24 deg/s: − 0.44; 28 deg/s: − 0.68; unpredictable: 0.02). The colored and black lines indicate the predictable and unpredictable conditions, respectively. The values in parentheses in the legend represent the number of trials included in each distribution.