Acute pain impairs retention of locomotor learning

Abstract

Despite abundant evidence that pain alters movement performance, considerably less is known about the potential effects of pain on motor learning. Some of the brain regions involved in pain processing are also responsible for specific aspects of motor learning, indicating that the two functions have the potential to interact, yet it is unclear if they do. In experiment 1, we compared the acquisition and retention of a novel locomotor pattern in young, healthy individuals randomized to either experience pain via capsaicin and heat applied to the lower leg during learning or no stimulus. On day 1, participants learned a new asymmetric walking pattern using distorted visual feedback, a paradigm known to involve mostly explicit re-aiming processes. Retention was tested 24 h later. Although there were no differences in day 1 acquisition between groups, individuals who experienced pain on day 1 demonstrated reduced retention on day 2. Furthermore, the degree of forgetting between days correlated with pain ratings during learning. In experiment 2, we examined the effects of a heat stimulus alone, which served as a control for (nonpainful) cutaneous stimulation, and found no effects on either acquisition or retention of learning. Thus, pain experienced during explicit, strategic locomotor learning interferes with motor memory consolidation processes and does so most likely through a pain mechanism and not an effect of distraction. These findings have important implications for understanding basic motor learning processes and for clinical rehabilitation, in which painful conditions are often treated through motor learning-based interventions.NEW & NOTEWORTHY Pain is a highly prevalent and burdensome experience that rehabilitation practitioners often treat using motor learning-based interventions. Here, we showed that experimental acute pain, but not a heat stimulus, during locomotor learning impaired 24-h retention of the newly learned walking pattern. The degree of retention loss was related to the perceived pain level during learning. These findings suggest important links between pain and motor learning that have significant implications for clinical rehabilitation.

Keywords: capsaicin; consolidation; locomotion; motor learning; walking.

Graphical abstract

Figure 1.

Experimental paradigm. A: treadmill walking setup: participants walked on a treadmill while viewing visual feedback of their step lengths on a monitor. Step lengths were depicted as vertical bars that grew in height in real time with each step. B: visual feedback: during practice periods, feedback was altered to drive learning of a novel asymmetric stepping pattern. Dotted line bars indicate the lengths of step actually taken (not visible to participants); solid bars indicate the step lengths with the gain included (shown to participants). Here, three sample time periods are shown for illustration purposes, but the visual feedback was provided continuously in real time. C: experimental timeline: blue and green shading indicate the key epochs during baseline, learning 1, and learning 2 blocks used for analysis. Participants were asked to rate their pain at the time points indicated with vertical arrows (pain ramp-up ratings not shown). BL, baseline; P, practice.

Figure 2.

Experiment 1. Day 1 pain ratings for the Pain group. Black horizontal bars indicate median pain ratings, shaded boxes indicate the interquartile ranges, and lower and upper whiskers indicate the minimum and maximum ratings, respectively. Open circles indicate outliers. BL, baseline; P, practice.

Figure 3.

Experiment 1. Step length asymmetry values (SLAs) shown on a stride-by-stride basis (in bins of 4 strides) for two exemplar participants, one each from the Pain (pink trace) and No Stimulus (blue trace) groups. Gray dashed horizontal lines indicate the target SLA. BL, baseline.

Figure 4.

Experiment 1. A: group average step length asymmetry values (SLAs) shown on a stride-by-stride basis (in bins of 4 strides) for the Pain group (pink trace) and No Stimulus group (blue trace). Data are truncated to the length of the individual with the shortest Practice period, with the final six bins shown for all (indicated by hatching on the x-axis). Gray dashed horizontal lines indicate the target SLA. Insets show the Late Practice 1, Late Practice 2, and Retention epochs. Shading indicates ±1 SE. BL, baseline. Group average SLAs at Late Practice 1, Late Practice 2, and Retention epochs (B), and group average forgetting indices for the Pain (pink squares) and No Stimulus (blue circles) groups (C). Error bars indicate ±1 SEM. *Significant pairwise comparison post hoc from the interaction effect. **Significant difference from the independent t test between groups.

Figure 5.

Experiment 1. Scatterplot showing the correlation between average pain rating and forgetting index for the Pain group.

Figure 6.

Experiment 2. Group average step length asymmetry values (SLAs) at Late Practice 1, Late Practice 2, and Retention epochs (A), and group average forgetting indices for the Heat Only (triangles) and No Stimulus (circles) groups (B). Error bars indicate ±1 SE.