The temporal evolution of feedback gains rapidly update to task demands

Abstract

Recent theoretical frameworks such as optimal feedback control suggest that feedback gains should modulate throughout a movement and be tuned to task demands. Here we measured the visuomotor feedback gain throughout the course of movements made to "near" or "far" targets in human subjects. The visuomotor gain showed a systematic modulation over the time course of the reach, with the gain peaking at the middle of the movement and dropping rapidly as the target is approached. This modulation depends primarily on the proportion of the movement remaining, rather than hand position, suggesting that the modulation is sensitive to task demands. Model-predictive control suggests that the gains should be continuously recomputed throughout a movement. To test this, we investigated whether feedback gains update when the task goal is altered during a movement, that is when the target of the reach jumped. We measured the visuomotor gain either simultaneously with the jump or 100 ms after the jump. The visuomotor gain nonspecifically reduced for all target jumps when measured synchronously with the jump. However, the visuomotor gain 100 ms later showed an appropriate modulation for the revised task goal by increasing for jumps that increased the distance to the target and reducing for jumps that decreased the distance. We conclude that visuomotor feedback gain shows a temporal evolution related to task demands and that this evolution can be flexibly recomputed within 100 ms to accommodate online modifications to task goals.

Figure 1.

Experimental paradigm. A, Subjects were seated with their right forearm resting on an air sled. They grasped the handle of a robotic manipulandum (vBOT) with their right hand. Direct view of their right arm was prevented by a mirror through which visual feedback from the monitor was overlaid in the plane of movement. B, The subjects' task was to make forward-reaching movements from a start point (filled gray circle) located ∼20 cm in front of the chest to a target (black circle) placed directly across the start point (i.e., on the y-axis). C, Throughout the study, a visual cursor was presented to the subject as a representation of their hand location. On probe trials, the cursor could jump either right or left by 3 cm (i.e., perpendicular to the principal axis of movement) for 250 ms (black trace). During these trials, the physical location of the hand (gray dotted trace) was constrained to move in a straight line toward the target by a mechanical channel produced by the vBOT. These trials were used to measure the magnitude of the visuomotor feedback response (which we term “gain”).

Figure 2.

Time course of visuomotor gain. A, Left: Subjects made forward-reaching movements to the near target (17.5 cm), whereas on random trials, the visual location of the hand was perturbed either left or right at one of seven locations during movement. Middle: Different colors correspond to the different perturbation onset locations during reaching. Lateral forces exerted on the force channel in response to perturbations of the visual location of the hand during movement to a “near” target for a single subject. Responses to left and right perturbations are combined for each perturbation location with appropriate sign so that corrective forces are positive. Zero time indicates the onset of the visual perturbation and the gray background represents the reflex time window for force. Right: Mean lateral forces exerted on the channel across all subjects. B, Lateral force responses to cursor perturbations when reaching to a “far” (25 cm) target. C, Magnitude of lateral forces over the involuntary time window in A and B averaged across subjects separately for movements to the near (black trace) and far (brown trace) target. In the left panel, magnitudes are plotted as a function of absolute position from the start point; in the middle panel, the magnitudes are plotted as a function of percentage distance to the target; and in the right panel, the magnitudes are plotted as a function of the forward velocity, where each of these measures is determined at the time of perturbation onset. The error bars (both vertical and horizontal) represent the SEM. During reaching to either target, the visuomotor reflex gain was highest during the middle of movement and then decreased sharply as the hand neared the target. Higher initial gains were observed when reaching to the near target compared with the far target. D, The magnitude of lateral forces over the involuntary time window in A and B for movements to the near (black trace) and far (brown trace) target plotted as a function of the mean absolute position from the start point, percentage of distance to the target, and forward velocity over the same involuntary time window (180–230 ms).

Figure 3.

Simultaneous target and visual hand location perturbations. In Experiment 2, subjects made forward-reaching movements to a target that was initially set 25 cm away (far target) or 17.5 cm away (near target). A, Experimental protocol of movements to the far target. On random trials, one of three probe trial types was applied. On these perturbation trials, either only the cursor was perturbed (red trace, left), only the target was perturbed from the far to the near location (black trace, middle), or both the target and cursor were perturbed (blue trace, right). The onset of all three perturbations occurred at the same distance of movement to the target (15.75 cm) (t_pert = t_jump). B, Hand position and lateral forces for single subject responses to visual perturbations for the three perturbation conditions during movements to the far target. C, Hand position and lateral forces for single subject responses during movements to the near target in which the target could jump to the far location. D, E, Force responses to visual perturbations averaged across subjects. Zero time indicates the onset of the perturbations (t_pert), shading represents the SEM, and gray rectangles indicate the visuomotor reflex time window. F, G, Averaged forces over the reflex time window. Error bars represent 1 SD. Significant difference from the post hoc tests are indicated (***p < 0.001, ** p < 0.01). Little if any lateral forces were produced in response to target perturbations alone (gray bar). There was a reduction in force magnitude when cursor perturbations were accompanied by a concurrent target perturbation (blue bar smaller than red) regardless of the direction of target displacement. H, I, Position and velocity across subjects for the three perturbation conditions at the time of the perturbation onset (time 0 ms) and over the response interval (180–230 ms). J, K, Electromyographic responses in the posterior deltoid to the three perturbation conditions during movements to the far and near targets. The responses are shown for cursor perturbations to the left (solid red trace), cursor perturbations to the right (dotted red trace), combined cursor perturbation to the left and target jump (solid blue trace), combined cursor perturbation to the right and target jump (dotted blue trace), and only target jumps (black trace). Responses are averaged across subjects and shaded regions represent SEM. The gray rectangle indicates the reflex time window for EMG (120–180 ms after perturbation onset).

Figure 4.

Delayed cursor perturbations. A, Experimental protocol of movements to the far target. On random trials, one of three probe trial types was applied. On these perturbation trials, either only the cursor was perturbed (red trace, left), only the target was perturbed from far to the near location (black trace, middle), or both the target and cursor was perturbed (blue trace, right). The onset of all target jumps occurred when subjects had moved 10.75 cm distance (at time t_jump), whereas cursor perturbations occurred when subjects had moved 15.75 cm to the target (at time t_pert). This led to an approximately 100 ms delay between the target jump and the cursor perturbation (t_pert = t_jump + ∼100 ms). B, Hand position and lateral forces for a single subject for movements to the far target. C, Hand position and lateral forces for a single subject for movements to the near target in which the target could jump to the far location. D, E, Force responses to visual perturbations averaged across subjects. Zero time indicates the onset of the cursor perturbations (t_pert), shading represents the SEM, and gray rectangles indicate the visuomotor reflex time window. F, G, Averaged forces over the reflex time window. Error bars represent 1 SD. Significant difference from the post hoc tests are indicated (***p < 0.001, ** p < 0.01). There was a reduction in force magnitude during movements to the far target when cursor perturbations were preceded by a target jump to the near location. However, there was an increase in force magnitude to cursor perturbations during movements to the near target when the cursor perturbation was preceded by a target jump to the far location. H, I, Position and velocity across subjects for the three perturbation conditions at the time of the perturbation onset (time 0 ms) and over the response interval (180–230 ms). J, K, Electromyographic responses in the posterior deltoid to the three perturbation conditions during movements to the far and near targets. The responses are shown for cursor perturbations to the left (solid red trace), cursor perturbations to the right (dotted red trace), combined cursor perturbation to the left and target jump (solid blue trace), combined cursor perturbation to the right and target jump (dotted blue trace), and only target jumps (black trace). Responses are averaged across subjects and shaded regions represent SEM. The gray rectangle indicates the reflex time window for EMG (120–180 ms after perturbation onset).