Visuomotor feedback gains upregulate during the learning of novel dynamics

Abstract

At an early stage of learning novel dynamics, changes in muscle activity are mainly due to corrective feedback responses. These feedback contributions to the overall motor command are gradually reduced as feedforward control is learned. The temporary increased use of feedback could arise simply from the large errors in early learning with either unaltered gains or even slightly downregulated gains, or from an upregulation of the feedback gains when feedforward prediction is insufficient. We therefore investigated whether the sensorimotor control system alters feedback gains during adaptation to a novel force field generated by a robotic manipulandum. To probe the feedback gains throughout learning, we measured the magnitude of involuntary rapid visuomotor responses to rapid shifts in the visual location of the hand during reaching movements. We found large increases in the magnitude of the rapid visuomotor response whenever the dynamics changed: both when the force field was first presented, and when it was removed. We confirmed that these changes in feedback gain are not simply a byproduct of the change in background load, by demonstrating that this rapid visuomotor response is not load sensitive. Our results suggest that when the sensorimotor control system experiences errors, it increases the gain of the visuomotor feedback pathways to deal with the unexpected disturbances until the feedforward controller learns the appropriate dynamics. We suggest that these feedback gains are upregulated with increased uncertainty in the knowledge of the dynamics to counteract any errors or disturbances and ensure accurate and skillful movements.

Fig. 1.

Experimental setup and protocol. A: the subject grasped the handle of the robotic manipulandum (vBOT) while seated. Visual feedback of movements was presented veridically using a top-mounted computer screen viewed through a mirror. The subject's forearm was fixed to the handle and supported by an airsled. B: visual perturbations (probe trials) were used to examine the magnitude of the visually induced motor response. On random movements throughout the experiments, the physical location of the hand (solid gray line) was constrained to a straight-line trajectory to the target using a mechanical channel (grey arrows). During these trials, at a location 6.25 cm from the start of the movement, the visual cursor representing the subject's hand (dotted black line) was displaced by 2.0 cm for 250 ms of the movement before being returned back to the actual hand position. C: learning was examined by introducing a velocity-dependent curl force field (CF). On a straight movement to the target, the force applied by this field to the subject's hand (gray arrows) varied with the forward movement velocity. For hand movements (black line) with a normal bell-shaped velocity profile, the forces are shown. D: to test the dependence of the rapid visuomotor response on background load, experiments were introduced in which a constant background load orthogonal to the direction of motion of various magnitudes was introduced. The load was applied before the movement onset and removed after subjects completed the movement. The forces applied to the hand (gray arrows) were constant in Cartesian coordinates regardless of the movement kinematics. E: experimental protocol in the learning experiment. Each of 5 different stages in the experiment consisted of 542 trials that alternated between forward and backward movements. Subjects proceeded through the experiment by first making movements in the null force field (NF; preexposure). The CF was then introduced over three stages of the experiment (CF exposure, 1,626 trials total). Finally, subjects again made movements in the NF (postexposure) to assess the degree of learning achieved in the force field. Probe trials to assess feedback gain were applied in four of the five stages.

Fig. 2.

Trajectory correlates of adaptation. A: data from one subject showing the forward movement paths in four stages during the learning experiment. The movement paths are shown for the last five movements in the preexposure NF (green), first five movements in the force field (early exposure stage, brown), last five movements in the force field (late exposure stage, orange), and first five movements in the postexposure stage (blue). B: data from one subject showing the backward movement paths in four stages during the learning experiment. C: maximum perpendicular error in the forward direction movements during the five stages of learning: preexposure (green), early exposure (brown), middle exposure (red), late exposure (orange), and postexposure (blue). The sold line represents the maximum perpendicular error across all subjects (mean value across all nonprobe trials within each block of the experiment). The colored shaded region shows the SE. The gray shaded bar indicates the period in which the CF was applied. D: mean values of maximum perpendicular error across all subjects in each block throughout the experiment during movements in the backward direction.

Fig. 3.

Electromyographic correlates of adaptation. A: integrated electromyographic activity of six arm muscles [mean (solid line) and SE (shaded region) across all eight subjects] during nonprobe trial movements in the forward direction during the five stages of the learning experiment: preexposure (green), early exposure (brown), middle exposure (red), late exposure (orange), and postexposure (blue). The gray shaded bar indicates the period in which the CF was applied. The green dotted line shows the mean muscle activity level in the last half of the preexposure NF trials for comparison. Muscles are arranged as antagonistic pairs (left to right: single joint shoulder muscles, biarticular muscles, and single joint elbow muscles) with flexor muscles on the top and extensor muscles on the bottom. B: integrated electromyographic activity of six arm muscles (mean across all eight subjects) during nonprobe trial movements in the backward direction during the five stages of the learning experiment.

Fig. 4.

Magnitude of rapid visuomotor responses during adaptation. A: force produced in response to a shift in the visual representation of hand position (probe) during forward movements in four stages of learning: preexposure (green), early exposure (brown), late exposure (orange), and postexposure (blue). Magnitude of force represents the difference between visual perturbations to the right and visual perturbation to the left. The solid line indicates the mean responses across subjects, and the shaded colored region represents the SE. The shaded bar shows the time interval (180–230 ms) over which the response was examined in B. B: mean force magnitude across all subjects in response to visual perturbation (left-right visual perturbation) during the 180- to 230-ms interval after the onset of the perturbation during movements in the forward direction. The black line indicates the SD of response magnitudes across all subjects. Significant differences, as assessed with Tukey's honest significant difference (HSD) post hoc test, are indicated (*P < 0.05; **P < 0.01; ***P < 0.001). C: force produced in response to a shift in the visual representation of hand position (probe) during backward movements in four stages of learning. D: mean force magnitude across all subjects in response to visual perturbation (left-right visual perturbation) during the 180- to 230-ms interval after the onset of the perturbation during movements in the backward direction.

Fig. 5.

Feedback correlates of adaptation. A: changes in the visuomotor feedback magnitude during blocks of probe trials throughout four stages of learning: preexposure (green), early exposure (brown), late exposure (orange), and postexposure (blue). The mean response over an early interval (180–230 ms after the visual perturbation onset) before voluntary action was calculated. The data shown are means (±SE) of eight subjects. Statistically significant differences between certain blocks across the stages were tested using Tukey's HSD post hoc test (*P < 0.05; **P < 0.01; ***P < 0.001). B: visuomotor feedback magnitude as a function of the mean maximum perpendicular error in each block. The first five blocks in the initial preexposure phase are not shown.

Fig. 6.

Comparison of end point force in the learning and constant background load experiments. A: end point force in the x-axis as a function of time in the NF (preexposure, green; postexposure, blue), CF (early exposure, brown; late exposure, orange), and constant background loads (2 N, light green; 4 N, dark green; 6 N, navy). The solid line indicates the mean, and the shaded region represents the SD of all nonprobe trials within a condition. B: position in the y-axis as a function of time for all of the conditions. Data are shown for a single subject who participated in both experiments.

Fig. 7.

Magnitude of rapid visuomotor responses during movement with constant background loads. In all elements shown, the scale is identical to the results in Fig. 4 for ease of comparison. A: force produced in response to a shift in the visual representation of hand position (probe) during movements with three different constant background loads applied in the direction lateral to motion (2 N, light green; 4 N, dark green; 6 N, navy). The magnitude of force represents the difference between visual perturbations to the right and visual perturbation to the left. The solid line indicates the mean responses across subjects, and the shaded colored region represents the SE. The shaded bar shows the time interval (180–230 ms) over which the response was examined in B. B: mean force magnitude across all subjects in response to visual perturbation (left-right visual perturbation) during the 180- to 230-ms interval after the onset of the perturbation during movements with constant lateral load. The black line indicates the SD of response magnitudes across all subjects. The P value indicates the result of ANOVA. C: visuomotor feedback magnitude as a function of the mean maximum perpendicular error in each block. The scale is identical to that of Fig. 5C.