Visuomotor Map Determines How Visually Guided Reaching Movements are Corrected Within and Across Trials

Abstract

When a visually guided reaching movement is unexpectedly perturbed, it is implicitly corrected in two ways: immediately after the perturbation by feedback control (online correction) and in the next movement by adjusting feedforward motor commands (offline correction or motor adaptation). Although recent studies have revealed a close relationship between feedback and feedforward controls, the nature of this relationship is not yet fully understood. Here, we show that both implicit online and offline movement corrections utilize the same visuomotor map for feedforward movement control that transforms the spatial location of visual objects into appropriate motor commands. First, we artificially distorted the visuomotor map by applying opposite visual rotations to the cursor representing the hand position while human participants reached for two different targets. This procedure implicitly altered the visuomotor map so that changes in the movement direction to the target location were more insensitive or more sensitive. Then, we examined how such visuomotor map distortion influenced online movement correction by suddenly changing the target location. The magnitude of online movement correction was altered according to the shape of the visuomotor map. We also examined offline movement correction; the aftereffect induced by visual rotation in the previous trial was modulated according to the shape of the visuomotor map. These results highlighted the importance of the visuomotor map as a foundation for implicit motor control mechanisms and the intimate relationship between feedforward control, feedback control, and motor adaptation.

Keywords: feedback control; feedforward control; motor adaptation; reaching movement; visuomotor map.

Figure 1.

Schematic representation of our hypothesis. The visuomotor map is the relationship between the target direction and hand movement direction. A, In ordinary situations, these two directions are almost identical. B, If the map can be distorted (represented by a blue solid line), a voluntary reaching movement toward three targets should always result in the same hand movement directed to 0°. Participants cannot voluntarily change the movement direction even if they try. C, D, We hypothesized that online movement correction to a target jump (C) and offline movement correction observed after imposing visual rotation (D) also cannot be changed appropriately.

Figure 2.

Experimental setup. Participants alternately reached toward one of two targets located rightward and leftward. A, In inward adaptation group, gradually increasing rightward and leftward visual rotations were imposed on the cursor when reaching to rightward and leftward targets, respectively. This procedure would make the handle movements closer to the target. Participants were not aware of the presence of visual rotation. B, In the outward adaptation group, the association of target and visual rotation was reversed, making the handle movements more distant. C–E, the participants performed probe trials in order to obtain the visuomotor map (C), online (D), and offline movement correction (E) in Experiments 1, 2, and 3, respectively (see Materials and Methods).

Figure 3.

Distortion of visuomotor map. A, B, The imposed visual rotation (solid lines) and the movement direction of the hand in the trial for inward (A) and outward adaptation groups (B). The hand movements became closer (A) and more distant (B) to compensate for gradually increasing visual rotation. Data are represented by mean ± SD. C, Visuomotor map before (broken lines) and after distortion (solid lines). The shape of the visuomotor map in the vicinity of the central target (0°) was distorted according to the training that each group received. Notably, movement toward the central target remained unchanged. Error bars represent SD.

Figure 4.

Online movement correction. A, B, Trajectories of the hand before (broken lines) and after (solid lines) distortion of the visuomotor map for the inward adaptation group (A) and outward adaptation group (B). Each color represents the trajectory for a discrete target jump. C, Online movement correction was evaluated 1000 ms after the onset of target jump before and after distortion of the visuomotor map. D, The slope of the linear relationship between size of the target jump and corrected movement direction (C) significantly decreased after distortion in the inward adaptation group, whereas it significantly increased in the outward adaptation group. Error bars indicate SD.

Figure 5.

Rapid component of online movement correction. A, B, The x-component of force output exerted on the handle before (broken lines) and after (solid lines) distortion of the visuomotor map for the inward (A) and outward (B) adaptation group. The values shown on the right side indicate the size of target jump. C, Force output was averaged between 170 and 200 ms after target jump for each size jump (small, dashed-dotted lines; medium, broke lines; large, solid lines). Error bars indicate SD.

Figure 6.

Kinematics of the movement. A, B, The trajectories of the handle during movement to the central target (the cursor was visible) before and after intervention for the inward (A) and for outward (B) adaptation groups are shown. Solid bold lines indicate the averaged trajectory of participants. Shaded areas indicate SD. Note that the scale for the x-direction is exaggerated. C, The handle’s x-position during peak velocity was quantified to examine the shape of the trajectories. After intervention, the values became significantly smaller by 1.9 mm only for the outward adaptation group, indicating that the trajectories were slightly curved leftward. D, The lateral deviation of the cursor’s direction at peak velocity from the target direction (left, central, and right targets) was quantified by taking the root mean squared value for each participant. After intervention, the deviation significantly increased only in the inward adaptation group. In C and D, error bards indicate SD.

Figure 7.

Offline movement correction. A, The aftereffect was quantified in the trial immediately after the perturbation trial (it was evaluated as the movement direction 120 ms after movement onset). The aftereffect significantly decreased after distortion of the visuomotor map in the inward adaptation group, whereas it significantly increased in the outward adaptation group. B, Visual errors in the perturbation trial (the errors should be 30º) were not significantly different before and after intervention. Error bars indicate SD.

Figure 8.

Online movement corrections in the perturbation trial in Experiment 3. A, B, The trajectory of the handle during movement to the central target in the perturbation trials, before and after the intervention, for the inward (A) and outward (B) adaptation groups is shown. The dotted circles indicate the corresponding final positions if movements were fully corrected. C, Online movement correction was evaluated 500 ms after movement onset, before and after distortion of the visuomotor map. D, The slope of the linear relationship between the size of the visual rotation and the corrected movement direction did not change by distorting the visuomotor map, for both experimental groups. Error bars indicate SD. E, F, The x-component of the force output exerted on the handle before (broken lines) and after (solid lines) distortion of the visuomotor map are shown for the inward (E) and outward (F) adaptation groups from movement onset.