Visuomotor feedback gains are modulated by gaze position

Abstract

During goal-directed reaching, people typically direct their gaze to the target before the start of the hand movement and maintain fixation until the hand arrives. This gaze strategy improves reach accuracy in two ways. It enables the use of central vision at the end of movement, and it allows the use of extraretinal information in guiding the hand to the target. Here we tested whether fixating the reach target further facilitates reach accuracy by optimizing the use of peripheral vision in detecting, and rapidly responding to, reach errors during the ongoing movement. We examined automatic visuomotor corrections in response to displacements of the cursor representing the hand position as a function of gaze fixation location during unimanual goal-directed reaching. Eight fixation targets were positioned either in line with, or at different angles relative to, the straight-ahead movement direction (manipulation of fixation angle), and at different distances from the location of the visual perturbation (manipulation of fixation distance). We found that corrections were fastest and strongest when gaze was directed at the reach target compared with when gaze was directed to a different location in the workspace. We found that the gain of the visuomotor response was strongly affected by fixation angle, and to a smaller extent by fixation distance, with lower gains as the angle or distance increased. We submit that fixating the reach target improves reach accuracy by facilitating rapid visuomotor responses to reach errors viewed in peripheral vision. NEW & NOTEWORTHY It is well known that directing gaze to the reach target allows the use of foveal visual feedback and extraretinal information to improve the accuracy of reaching movements. Here we demonstrate that target fixation also optimizes rapid visuomotor corrections to reach errors viewed in peripheral vision, with the angle of gaze relative to the hand movement being a critical determinant in the gain of the visuomotor response.

Keywords: eye movements; motor control; online corrections; reaching; vision.

Fig. 1.

Experimental setup and task. A: participants performed reaching movements in the horizontal plane while holding onto a robotic manipulandum. B: example nonchannel perturbation trial. Participants reached from a start position to a narrow (blue) or wide (red) reach target while fixating their gaze at a fixation target (gray circle). On a subset of trials, the hand cursor was visually perturbed by displacing it 3 cm to the left or right after it passed under a visual occluder. C: example force channel trial. In one-half of the trials, the participants’ movements were constrained along a straight line from the start to target position, allowing us to measure the forces applied to the virtual walls of the channel (broken lines). In cursor perturbation trials, the cursor automatically moved back to this line 250 ms after the perturbation. D: fixation targets were placed at different distances (12.5 cm, “near”; 22.5 cm, “far”) from the perturbation location and at different angles (0°, ±45°, ±90°) with respect to the movement direction.

Fig. 2.

Raw data of an example participant. A: cursor paths in response to a leftward (blue and red), no (gray), or rightward (green and orange) perturbation of the hand cursor during reaches to narrow (1st and 3rd row) and wide (2nd and 4th row) targets in trials without a force channel. B: forces measured in channel trials in response to a leftward (blue and red) or rightward (green and orange) perturbation of the hand cursor during reaches to narrow (1st and 3rd row) and wide (2nd and 4th row) targets. Thin traces indicate the forces on individual trials, thick traces indicate the average force. The gray shaded area indicates the 180- to 230-ms interval across which the force differences were averaged to obtain a single measure of the strength of the response.

Fig. 3.

Group-averaged results. Blue dots and lines correspond to reaches to narrow targets; red dots and lines correspond to reaches to wide targets. Continuous lines and filled dots correspond to “near” fixation targets (12.5 cm from the point where the cursor, on average, exits the occluder); dotted lines and open dots correspond to “far” fixation targets (22.5 cm from the perturbation point). A: mean force differences averaged across the 180- to 230-ms interval following cursor perturbation, as a function of the angle of fixation relative to the movement direction in the horizontal plane (see inset). B: mean onset of the corrective force response (see Data Analysis) as a function of fixation angle. C: mean force differences as in A, as a function of the distance between the perturbation point and the fixation target in visual angle (see Data Analysis). Labels indicate the angle of fixation relative to the movement direction in Cartesian coordinates. D: mean variability in the horizontal coordinate of the reach end point in nonchannel trials, as a function of fixation angle. E: mean duration between the perturbation and the cursor reaching the target in nonchannel trials, as a function of fixation angle.