Mirror reversal and visual rotation are learned and consolidated via separate mechanisms: recalibrating or learning de novo?

Abstract

Motor learning tasks are often classified into adaptation tasks, which involve the recalibration of an existing control policy (the mapping that determines both feedforward and feedback commands), and skill-learning tasks, requiring the acquisition of new control policies. We show here that this distinction also applies to two different visuomotor transformations during reaching in humans: Mirror-reversal (left-right reversal over a mid-sagittal axis) of visual feedback versus rotation of visual feedback around the movement origin. During mirror-reversal learning, correct movement initiation (feedforward commands) and online corrections (feedback responses) were only generated at longer latencies. The earliest responses were directed into a nonmirrored direction, even after two training sessions. In contrast, for visual rotation learning, no dependency of directional error on reaction time emerged, and fast feedback responses to visual displacements of the cursor were immediately adapted. These results suggest that the motor system acquires a new control policy for mirror reversal, which initially requires extra processing time, while it recalibrates an existing control policy for visual rotations, exploiting established fast computational processes. Importantly, memory for visual rotation decayed between sessions, whereas memory for mirror reversals showed offline gains, leading to better performance at the beginning of the second session than in the end of the first. With shifts in time-accuracy tradeoff and offline gains, mirror-reversal learning shares common features with other skill-learning tasks. We suggest that different neuronal mechanisms underlie the recalibration of an existing versus acquisition of a new control policy and that offline gains between sessions are a characteristic of latter.

Keywords: consolidation; mirror reversal; reaching movements; sensorimotor adaptation; skill learning; visual rotation.

Figure 1.

Schematic drawing of recalibration during MR and VR. The hyphenated vertical line indicates the mirror reversal axis. In trial n, hand (red) movements toward the −20° target (Fig. 2 for coordinate frame) result in the cursor (blue) traveling to 20°, thus producing an error (hyphenated black arrow) of 40°. A fraction of this error vector is used to update the next motor command. On trial n + 1, the hand movement direction (solid red arrow) is therefore shifted from the previous movement direction (hyphenated red arrow). During VR (top), this leads to error reduction between cursor (solid blue arrow) and target compared with the previous movement. During MR (bottom), the same update results in an increased error.

Figure 2.

Target arrangements in Experiments 1 and 2. Gray circles represent target locations in Experiment 1, whereas white circles represent target locations in Experiment 2. Targets at 0° and 180° are half-gray/half-white because they were presented in both experiments. The hyphenated vertical line indicates the mirror reversal axis in Experiment 1. In Experiment 2, the rotations were applied relative to the start location.

Figure 3.

Group-average reaction time across Experiments 1 and 2. White background represents reaching under normal visual feedback, whereas gray background represents reaching during mirror reversed or rotated visual feedback. The vertical line indicates the break between sessions. A, RT for −160°, −20°, 20°, and 160° targets during mirror reversal learning (Experiment 1). B, RT for reaching toward 8 targets during VR (Experiment 2). Error bars indicate between-subject SE.

Figure 4.

Relationship between RT and the directional error in Experiments 1 and 2. Blocks 1–4 were collected during baseline and blocks 5–24 during MR or VR. The trials were binned by RT for each target, participant, and block. Visual feedback was veridical during blocks 1–4 and mirror reversed or rotated during blocks 5–24. Blocks 1–12 were measured during the first session, blocks 13–24 during the second session. A, Mirror reversal: visual errors from movements toward the −160° and 20° target were flipped to allow averaging with errors from the −20° and 160° targets. Visual errors <20° indicate that the hand reached into the wrong (unmirrored) direction. Completely unadapted responses would yield an error of 40°. B, Visual rotation. A completely unadapted response would result in an error of 40°. Error bars indicate between-subject SE.

Figure 5.

Relationship between time and feedback response during mirror reversal learning (Experiment 3). Shown is the force measured in the channel produced in reaction to a 1.5 cm cursor displacement. Blocks 1–4 were collected during baseline and blocks 5–24 during MR. The hyphenated line indicates the reversed baseline response to serve as an illustration of what a perfectly mirror reversed feedback response would have looked like. Shaded area represents between-subject SE.

Figure 6.

Feedback responses in Experiments 4 and 5. A, In Experiment 5, the cursor (hyphenated gray line) and the hand (solid gray line) moved in the same direction. The cursor was displaced (hyphenated colored arrows) at an angle of −90° (dark blue), − 30° (light blue), 90° (red), or 150° (orange) relative to the movement direction. Displacements also occurred in 30° and −150° directions (data not shown). The hand movements that cancel out the cursor displacements are shown as solid arrows of the same color. B, In Experiment 4, the cursor (hyphenated gray line) was rotated by 60° or −60° (only the 60° is shown in the schematic) from the hand movement (solid gray line). Displacements were −90° (blue hyphenated) or 90° (red hyphenated) relative to the movement direction of the cursor. The solid red and dark blue arrows indicate the required hand movement directions that cancel out the corresponding displacement (hyphenated arrow with the same color). The orange and the light blue arrows represent what an unadapted response would look like. C, Quiver plot of feedback responses in Experiment 5 to −90° (dark blue) and 90° (red) cursor displacements. The vector origin represents the average hand position at time points from 75 to 375 ms after the cursor displacement (20 ms resolution), and the vector the difference in instantaneous hand velocity between trials with and without displacement. D, Feedback responses to −30° (light blue) and 150° (orange) cursor displacements in Experiment 5. E, Response to −90° (dark blue) and 90° (red) cursor displacements during baseline reaching (i.e., before cursor rotation in Experiment 4) and (F) with rotated cursor (blocks 5–8). Results are shown averaged over the 60° and −60° rotation groups, by right-left flipping the results for the −60° group. G, Mean angular direction of feedback correction (±SE) 250–350 ms after the displacement plotted over all blocks of Experiment 4. Responses are combined across cursor displacements and rotation groups. Light blue background represents blocks with visual rotation. Blue line and shading represent prediction of fully unadapted feedback response, based on mean and SE of responses to oblique cursor displacement in Experiment 5. H, Mean angular error of the feedforward command (±SE) averaged from 100 to 150 ms after movement onset while adapting to the 60° rotation in Experiment 4 for comparison.

Figure 7.

Consolidation of the feedforward command in Experiments 2 and 3. Average angular errors 100–150 ms after movement onset are plotted over the different blocks of the experiment (A–D) for the four mirror reversal groups (Experiment 3) and (E) the visual rotation group (Experiment 2). The error is corrected for the influence of time-accuracy tradeoff by calculating the average error at RT = 250 ms (see Materials and Methods). Colored background represents blocks with mirror reversal or visual rotation. The vertical hyphenated line separates the two sessions. All mirror reversal groups performed as well or better in the first block of the second session than in the last block of the first session. F, Bar graph of the difference in error between the first block in the second session (block 13) and the last block in the first session (block 12) split up by the visual rotation and the four mirror reversal groups: ME, EM, EE, MM; and the VR group. *p < 0.05 (significant t test against 0). Error bars indicate between-subject SE.

Figure 8.

Consolidation of the feedback command in Experiment 3. The average feedback command 250–350 ms after the displacement is plotted over different blocks of the experiment. Colored background represents mirror reversal of the visual feedback. A–D, Feedback commands of the four mirror reversal groups. E, Bar graph of the force differences between the first block in the second session (block 13) and the last block in the first session (block 12) split up by the four groups: ME, EM, EE, and MM. *p < 0.05 (significant t test against zero). Error bars indicate between-subject SE.