Effect of tonic pain on motor acquisition and retention while learning to reach in a force field

Abstract

Most patients receiving intensive rehabilitation to improve their upper limb function experience pain. Despite this, the impact of pain on the ability to learn a specific motor task is still unknown. The aim of this study was to determine whether the presence of experimental tonic pain interferes with the acquisition and retention stages of motor learning associated with training in a reaching task. Twenty-nine healthy subjects were randomized to either a Control or Pain Group (receiving topical capsaicin cream on the upper arm during training on Day 1). On two consecutive days, subjects made ballistic movements towards two targets (NEAR/FAR) using a robotized exoskeleton. On Day 1, the task was performed without (baseline) and with a force field (adaptation). The adaptation task was repeated on Day 2. Task performance was assessed using index distance from the target at the end of the reaching movement. Motor planning was assessed using initial angle of deviation of index trajectory from a straight line to the target. Results show that tonic pain did not affect baseline reaching. Both groups improved task performance across time (p<0.001), but the Pain group showed a larger final error (under-compensation) than the Control group for the FAR target (p = 0.030) during both acquisition and retention. Moreover, a Group x Time interaction (p = 0.028) was observed on initial angle of deviation, suggesting that subjects with Pain made larger adjustments in the feedforward component of the movement over time. Interestingly, behaviour of the Pain group was very stable from the end of Day 1 (with pain) to the beginning of Day 2 (pain-free), indicating that the differences observed could not solely be explained by the impact of pain on immediate performance. This suggests that if people learn to move differently in the presence of pain, they might maintain this altered strategy over time.

Figure 1. Experimental set-up and design.

Panel A - Subjects made right arm ballistic reaching movements to visual targets using the KINARM robotic exoskeleton. The zone on the upper arm where the capsaicin was applied is shown. Panel B - On Day 1, two blocks of baseline measurements (without force field) were recorded for both groups. The Acquisition period (with force field perturbation) began immediately after the end of Baseline 2. On Day 2, only one block with the force field was performed to evaluate the Retention. Each block includes 50 trials/target. For the Pain group, the red indicates when the capsaicin was present (single application between Baseline 1 and 2).

Figure 2. Selected kinematic variables.

This figure depicts the kinematic variables extracted from index finger trajectories, using examples of typical trials early in the Acquisition period (i.e. trajectories are strongly deviated in the direction of the force field). The fERR is measured as the distance between the index and the target when the index crossed the invisible 10-cm radius circle centered on the starting position. The iANG is computed as the angle between: 1) a line joining the position of the index at movement onset and the target; and 2) another line joining the position of the index at movement onset and at its first peak of acceleration.

Figure 3. Changes in mean error (fERR) across time for each group.

Panel A shows the time course for the FAR target, and Panel B for the NEAR target. Panels C and D show the average fERR for each group on sections of the time course selected for statistical analyses (Early/Late Day 1 and Late Day 2), respectively for FAR and NEAR target. Both groups improved their performance on Day 1, as illustrated by the rapid decay of fERR over trials. A strong Retention is demonstrated by a better performance on Early Day 2 compared to Early Day 1. However while both groups show very similar performance for the NEAR target, the Pain group systematically shows larger errors for the FAR target. This difference is still observed on Day 2, when all subjects are tested pain-free. Error bars show the standard error of mean (SEM).

Figure 4. Changes in initial angle of deviation (iANG) across time for each group.

Panel A shows the time course for the FAR target, and Panel B for the NEAR target. Panels C and D shows the average iANG for each group on sections of the time course selected for statistical analyses (Early/Late Day 1 and Late Day 2), respectively for FAR and NEAR target. On Day 1, both groups exhibited a reversal of the direction of their iANG: early in the force field their hand was deflected in the direction of the force field (negative angle value). Progressively, the movement was initiated in the opposite direction in anticipation of the perturbation. At the beginning of Day 2 iANG direction was opposite to the deviation produced by the force field and similar to what was seen at the end of Day 1, demonstrating the retention of the feedforward strategy acquired on Day 1. Error bars show the standard error of mean (SEM).