Reexposure to a sensorimotor perturbation produces opposite effects on explicit and implicit learning processes

Abstract

The motor system demonstrates an exquisite ability to adapt to changes in the environment and to quickly reset when these changes prove transient. If similar environmental changes are encountered in the future, learning may be faster, a phenomenon known as savings. In studies of sensorimotor learning, a central component of savings is attributed to the explicit recall of the task structure and appropriate compensatory strategies. Whether implicit adaptation also contributes to savings remains subject to debate. We tackled this question by measuring, in parallel, explicit and implicit adaptive responses in a visuomotor rotation task, employing a protocol that typically elicits savings. While the initial rate of learning was faster in the second exposure to the perturbation, an analysis decomposing the 2 processes showed the benefit to be solely associated with explicit re-aiming. Surprisingly, we found a significant decrease after relearning in aftereffect magnitudes during no-feedback trials, a direct measure of implicit adaptation. In a second experiment, we isolated implicit adaptation using clamped visual feedback, a method known to eliminate the contribution of explicit learning processes. Consistent with the results of the first experiment, participants exhibited a marked reduction in the adaptation function, as well as an attenuated aftereffect when relearning from the clamped feedback. Motivated by these results, we reanalyzed data from prior studies and observed a consistent, yet unappreciated pattern of attenuation of implicit adaptation during relearning. These results indicate that explicit and implicit sensorimotor processes exhibit opposite effects upon relearning: Explicit learning shows savings, while implicit adaptation becomes attenuated.

Fig 1. Experiment 1: Upon relearning a visuomotor rotation, explicit strategies show savings while implicit adaptation is attenuated.

(A) Task-level schematics of all trial types. (B) Time course of mean hand angle averaged over cycles (4 movements) when participants (N = 24) were asked to aim for the target (blue), either during No-Feedback blocks (No FB Baseline and Aftereffect, gray background), Veridical Feedback blocks (FB Baseline and Washout), or No-Feedback Probe trials and when asked to compensate for a rotated cursor (Rotation, pink). Light and dark colors signify blocks 1 and 2 of the experiment. Dotted vertical lines denote 1 (thin) and 2 (thick) min breaks. The labels “Early” and “Late” mark the cycles used for operationalizing measures of early and late learning. (C, D) To highlight changes across blocks, overlaid hand angle functions of blocks 1 and 2 for overall learning (explicit and implicit, Rotation trials, C) and implicit adaptation (Baseline, Probe and Aftereffect trials, D). Horizontal thick black lines mark clusters of cycles that show significant difference between the blocks with p < 0.05 probability. Cycle numbers in both C and D correspond to the cycles of the Rotation trials. (E–I) Summary analysis of Early learning (E, G) and Late learning (F, H) for the Rotation (E, F) and Probe (G, H) conditions, and of the aftereffects (I). Left pair of bars show the mean across participants for each block, and right bar shows the mean of the within-participant differences (Block 2 –Block 1). Black dots indicate individual difference scores. For all figure panels, shaded margins and black vertical lines represent SEM. The individual data and the summary statistics presented in this figure can be found in S1 Data. The raw data can be found in https://git.io/Jtiip. SEM, standard error of the mean.

Fig 2. Experiment 2: Task-irrelevant clamped feedback revealed an overall attenuation of implicit adaptation upon relearning.

(A) Task-level schematics of all trial types. (B) Experimental protocol of 2 experimental groups: Test (N = 16, green) and Control (N = 16, purple). For the Test group, the green oblique lines in the Washout block represent a transition from a reversed-clamp phase to a veridical feedback phase; the cycle of the transition was determined based on each individual’s performance in the reversed-clamp phase (see Methods). (C) Time courses of mean hand angle averaged over cycles (4 movements) for both groups. For the Test group, light and dark green colors signify blocks 1 and 2 of the experiment, with the onset of the task-irrelevant clamped feedback marked by the vertical solid lines. Dotted vertical lines denote 1 (thin) and 2 (thick) min breaks. The labels “Early” and “Late” mark the cycles used for operationalizing measures of early and late learning. (D) Overlaid hand angle functions for the 2 blocks. Horizontal thick black lines denote clusters that show a significant difference between blocks 1 and 2 (p < 0.05). (E–H) Summary analysis of Early learning (E), Late learning (F), and Aftereffect (G) stages for the Test group and Late learning for the Control group (H). Left pair of bars show the mean across participants for each block, and right bar shows the mean of the within-participant differences (Block 2 –Block 1). Black dots indicate individual difference scores. (I) Summary analysis comparing the Aftereffect between the groups in the last No FB block. Black dots represent data of individual participants. (J) Overlaid hand angle functions for the Aftereffect block of the Control group and the Aftereffect 1 (left panel) or Aftereffect 2 (right panel) of the Test group. For all figure panels, shaded margins and black vertical lines represent SEM. The individual data and the summary statistics presented in this figure can be found in S1 Data. The raw data can be found in https://git.io/Jtiip. SEM, standard error of the mean.

Fig 3. Prior evidence for attenuation upon relearning for implicit visuomotor adaptation.

(A) Cohen’s d effect size of the differences in learning measures between the second and first learning blocks for experiments meeting our criterion for inclusion in the review of the literature. Early learning (green circles), Late learning (blue triangles), Aftereffect (purple squares), and Learning rate (dark purple stars). (B, C) Overlaid hand angle functions of implicit adaptation to a visuomotor rotation over 2 learning blocks. Light and dark colors denote blocks 1 and 2 of the experiment, respectively. Shaded margins represent the SEM. In B, implicit adaptation was extracted by subtracting a reported aiming location from movement hand angle on every trial. Adapted with permission from Yin and Wei (2020). In C, implicit adaptive response to the rotated cursor when the target jumps in a manner that eliminates task error. Adapted with permission from Leow et al. (2020). (D) Learning rate during adaptation to a gradually changing visuomotor rotation, tested on 2 days. Pink markers represent individual participants. Black diagonal dotted line represents the unity line. Bars and black vertical lines (inset) represent mean and SEM, respectively. Adapted with permission from Stark-Inbar et al. (2016). The individual data and the summary statistics presented in this figure can be found in S1 Data. SEM, standard error of the mean.