Characteristics of Implicit Sensorimotor Adaptation Revealed by Task-irrelevant Clamped Feedback

Abstract

Sensorimotor adaptation occurs when there is a discrepancy between the expected and actual sensory consequences of a movement. This learning can be precisely measured, but its source has been hard to pin down because standard adaptation tasks introduce two potential learning signals: task performance errors and sensory prediction errors. Here we employed a new method that induces sensory prediction errors without task performance errors. This method combines the use of clamped visual feedback that is angularly offset from the target and independent of the direction of motion, along with instructions to ignore this feedback while reaching to targets. Despite these instructions, participants unknowingly showed robust adaptation of their movements. This adaptation was similar to that observed with standard methods, showing sign dependence, local generalization, and cerebellar dependency. Surprisingly, adaptation rate and magnitude were invariant across a large range of offsets. Collectively, our results challenge current models of adaptation and demonstrate that behavior observed in many studies of adaptation reflect the composite effects of task performance and sensory prediction errors.

Figure 1

A new method to induce implicit visuomotor adaptation. (A) Participants made center-out reaches on a digitizing tablet while grasping a stylus. (B) Illustration of the two visual feedback manipulations. For visuomotor rotations, the visual feedback is contingent on the hand movement. Clamped visual feedback breaks this contingency, with the feedback the same for all hand movements. Both types of feedback can be made irrelevant to the task with explicit instructions, but the error signal remains invariant with clamped visual feedback. (C) Behavior over all movement cycles for the Compensate, Ignore, and Clamp groups. (D) Baseline-adjusted mean hand angle over the last cycle of the perturbation block and the no-feedback aftereffect cycle. Dots are individual means; lines indicate group mean ± SEM. Gray shading denotes cycles without visual feedback.

Figure 2

Aftereffects and generalization are similar following exposure to a standard visuomotor rotation and a clamped visual feedback. (A) Task trial design. Participants reached to all targets for every phase of the experiment, except for the perturbation block in which all reaches were to a single target. (B) Behavior at the training target during each phase of the experiment. Both groups show a change in heading angle in response to the visual feedback perturbation, with the rotation group changing hand angle by an additional 8°. However, there was no difference once the perturbation was removed. (C) Baseline subtracted aftereffect at all targets. The generalization functions are remarkably similar for the two groups around the workspace. Values are group means; shading and error bars denote SEM. Gray shading denotes cycles without visual feedback.

Figure 3

Adaptation to a task-irrelevant clamped visual feedback is attenuated in patients with cerebellar degeneration. (A) Behavior for patients and controls over all movement cycles (4 reaches/cycle). (B) Adaptation over the last 10 cycles of the perturbation block showing both group lines indicate group mean ± SEM and individual hand angle values (dots, horizontally displaced for visualization). Gray shading denotes cycles without visual feedback.

Figure 4

Adaptation to clamped visual feedback does not scale with error size. (A) Color coding for clamped visual feedback of different offsets. Note that targets appeared at one of eight positions on a given trial. (B) Behavior for all groups, with data averaged over movements to all eight targets for each cycle. (C) Sensorimotor aftereffects, measured immediately following the perturbation block. (D) Per-trial adaptation rate over the first 10 cycles (80 trials) of the clamped visual feedback block. Dots are individual means; lines indicate group mean ± SEM. Gray shading denotes cycles without visual feedback.

Figure 5

Visual prediction error, contingent or not, drives adaptation. (A–C) Behavior over all movement cycles for each group with rotated feedback, presented with the corresponding clamped data from Experiment 3. (D) Sensorimotor aftereffects for all groups. Only the 7.5° group shows a difference between perturbation types. Dots are individual means; lines indicate group mean ± SEM. Gray shading denotes cycles without visual feedback.