Motor force field learning influences visual processing of target motion

Abstract

There are reciprocal connections between visual and motor areas of the cerebral cortex. Although recent studies have provided intriguing new insights, in comparison with volume of research on the visual control of movement, relatively little is known about how movement influences vision. The motor system is perfectly suited to learn about environmental forces. Does environmental force information, learned by the motor system, influence visual processing? Here, we show that learning to compensate for a force applied to the hand influenced how participants predicted target motion for interception. Ss trained in one of three constant force fields by making reaching movements while holding a robotic manipulandum. The robot applied forces in a null [null force field (NFF)], leftward [leftward force field (LFF)], or [rightward force field (RFF)] direction. Training was followed immediately with an interception task. The target accelerated from left to right and Ss's task was to stab it. When viewing time was optimal for prediction, the RFF group initiated their responses earlier and hit more targets, and the LFF group initiated their responses later and hit fewer targets, than the NFF group. In follow-up experiments, we show that motor learning is necessary, and we rule out the possibility that explicit force direction information drives how Ss altered their predictions of visual motion. Environmental force information, acquired by motor learning, influenced how the motion of nearby visual targets was predicted.

Figure 1.

Experimental tasks and scoring routines. A, The stimuli and response apparatus used for the force training task. The participant grasped the robotic manipulandum and used it to move a small black cursor to targets presented on a horizontal display. The blue rectangle represents the rest position in which there were no forces applied to the hand. The green square represents one of three start positions. Force magnitude increased as a function of the cursor position between the home position and the start position. The red dots reflect the arrangement of the three potential targets around each start position. B, Maximum perpendicular displacement for one trial. C, The stimulus and response apparatus used for the interception task. The participant moved the cursor into the green square start position on the right side of the screen while resisting the force in which they had trained. The target moved from left to right and participants either made a quick, jabbing movement to intercept the target directly in front of the hand starting position (interactive interception task) or they pressed a button with their left hand when they judged the target to be directly in front of their hand. D, The IP and interception zone used to determine our measure of timing error and interception success, respectively. ITD was defined as the difference in time when the center of the target passed x-coordinate of the IP and when the hand cursor passed the y-coordinate of the IP. Finally, an interception response was deemed successful if (any part of) the target and the hand cursor were in the interception zone concurrently.

Figure 2.

Results of force field training. A, Maximum perpendicular displacement (PD) (in millimeters) is shown as a function of force field direction (left, null, and right) and time in training. Over the first nine trials, force direction significantly influenced the direction and magnitude of PD. By trial 10, however, PD no longer depended on force field direction. B, Bars represent mean perpendicular displacement over the first nine trials (early) and the last nine trials (late) of training. Early in training, force direction significantly influenced the direction and magnitude of PD. By the end of training, however, PD no longer depended on force field direction. In each panel, error bars represent the SEM, and asterisks depict significant differences between means.

Figure 3.

Interception success, timing error, and spatial error for the interactive interception task. A, Interception success expressed as the percentage of targets hit as a function of FF direction. Participants who trained in the left FF hit significantly fewer targets than participants in the null FF, and participants who trained in the right FF hit significantly more targets than participants in the null FF. B, ITD as a function of FF direction. Participants who trained in the right FF missed the target by less time than participants who trained in the null or left FFs. C, ITD for misses as a function of viewing time and force direction. Under short viewing time conditions (472 ms), force direction does not influence ITD. In our longest viewing time condition (672 ms), ITD for the right FF group is significantly earlier than that for the null FF group, and ITD for the left FF group is significantly later than that for the null FF group. D, Spatial error for both hits and misses. For hits, hand spatial error was small and did not differ between force direction groups in either the X or Y dimensions. On trials counted as misses, there were significant differences between the FF groups along the Y (depth) dimension but not the X (horizontal) dimension, such that the left FF group missed the target by a greater distance than the null FF group, and the right FF group missed the target by a smaller distance than the null FF group. Error bars represent the SEM, and asterisks represent significant differences between means.

Figure 4.

Movement paths and movement times for interceptive movements made in experiment 1. A, Movement paths for interception movements made between the start position and the upper limit of the interception zone by both the left (black) and right (gray) FF groups. There is no significant difference in the horizontal position achieved by the two groups at the end of the movement. B, Interception movement path curvature or displacement (in millimeters) for the left (black), null (white), and right (gray) FF groups. C, Interception movement time (MT) (in milliseconds) as a function of force field direction. Like during training, MT for the null group (white) is significantly lower than that for the left (black) or right (gray) FF groups. There is no difference between the left and right FF groups. In each panel, error bars represent the SEM, and asterisks depict significant differences between means.

Figure 5.

Timing error and success rates for the button press interception task used in experiment 2. A, ITD as a function of FF direction. Participants who trained in the right FF timed interception earlier than participants who trained in the null or left FFs. B, Interception success expressed as the percentage of targets hit as a function of FF direction. In each panel, error bars represent the SEM, and asterisks depict significant differences between means.

Figure 6.

The histogram (dotted line) and mean (solid line) responses of participants' explicit postexperiment estimates of the directions in which the robot pushed their hand. The histogram was bimodal with modes centering on the 0° (right) and 180° (left) positions. The means of all responses on the left and right sides of the vertical meridian are depicted by the solid black and gray lines, respectively.