Two ways to save a newly learned motor pattern

Abstract

Savings, or faster relearning after initial learning, demonstrates humans' remarkable ability to retain learned movements amid changing environments. This is important within the context of locomotion, as the ability of the nervous system to "remember" how to walk in specific environments enables us to navigate changing terrains and progressively improve gait patterns with rehabilitation. Here, we used a split-belt treadmill to study precisely how people save newly learned walking patterns. In Experiment 1, we investigated savings by systematically varying the learning and unlearning environments. Savings was predominantly influenced by 1) previous exposure to similar abrupt changes in the environment and 2) the amount of exposure to the new environment. Relearning was fastest when these two factors coincided, and we did not observe savings after the environment was introduced gradually during initial learning. In Experiment 2, we then studied whether people store explicit information about different walking environments that mirrors savings of a new walking pattern. Like savings, we found that previous exposure to abrupt changes in the environment also drove the ability to recall a previously experienced walking environment accurately. Crucially, the information recalled was extrinsic information about the learning environment (i.e., treadmill speeds) and not intrinsic information about the walking pattern itself. We conclude that simply learning a new walking pattern is not enough for long-term savings; rather, savings of a learned walking pattern involves recall of the environment or extended training at the learned state.

Keywords: adaptation; gait; motor learning; savings; split-belt treadmill.

Fig. 1.

Experiment 1 protocol diagrams are shown for the Abrupt (A), Gradual (B), Gradual Washout (C), Extended Gradual (D), and Short Abrupt (E) groups. Dashed and solid lines indicate the speeds of the fast and slow belts, respectively. Colors assigned to each group will remain consistent throughout the figures.

Fig. 2.

A: general experimental setup for the Experiment 2 baseline and split recall tasks. Participants wore noise-canceling headphones and blinders while using a handheld button box to control the right belt speed of the treadmill. Experiment 2 protocol diagrams are also shown for the Abrupt (B), Gradual (C), Extended Gradual (D), Opposite Abrupt (E), and Short Abrupt (F) groups. The dashed red line indicates the speed of the right belt, whereas the solid black line indicates the speed of the left belt. Blue text indicates that the participant performed a recall task (slow and fast baseline recall tasks were performed in a randomized order across participants within each group).

Fig. 3.

Comparison of step length (SL) asymmetry during baseline, adaptation 1, and deadaptation among groups that adapted abruptly (Abrupt, orange; Gradual Washout, green; Short Abrupt, pink) (A) and adapted gradually (Gradual, black; Extended Gradual, blue) (B). Mean curves across participants within each group ± SE are shown. The curves are truncated in length to match the participant that took the fewest strides during each condition. Data points immediately following each adaptation 1 and deadaptation curve show the step length asymmetry during plateau (mean ± SE of the last 30 strides) for each group. Note that the adaptation 1 plateau for the Short Abrupt group was calculated as the mean of the last 5 strides. C: column graphs are shown indicating step length asymmetry during initial perturbation (mean of the first 5 strides), early change (mean of strides 6–30), and plateau of adaptation 1 (left) and deadaptation (right) for each group (mean ± SE). Gray boxes around the protocol diagrams included on the top right of each set of curves outline the portions of the protocol from which the data are presented. The statistical analyses are included in results.

Fig. 4.

Comparison of step length asymmetry during adaptation 2 (i.e., savings). Mean curves across participants within each group ± SE are shown. Note that the curves are truncated in length to match the participant that took the fewest strides during adaptation 2. Rows of plots are organized to indicate groups exhibiting no savings (top), savings during both initial perturbation and early change (middle), and savings during early change but not initial perturbation (bottom). Differences among groups during initial perturbation and early change are shown in the column graphs in the top right. A: Gradual (black) is compared with naïve abrupt adaptation data from the 28 participants in Abrupt and Gradual Washout during adaptation 1 (red). Embedded above the curves are column graphs indicating step length asymmetry during initial perturbation and early change. As Gradual performed similarly to naïve adaptation (i.e., no savings), we show all other groups relative to Gradual in B–E to demonstrate savings. Gray outlines behind the protocol diagrams included on the top right of each set of curves outline the portion of the protocol from which the data are presented. B: Abrupt (orange) is compared with Gradual (black). C: Gradual Washout (green) is compared with Gradual (black). D: Extended Gradual (blue) is compared with Gradual (black). E: Short Abrupt (pink) is compared with Gradual (black). Mean ± SE plateau values are plotted after each curve. There were no significant differences among groups in plateau during adaptation 2. *P < 0.05.

Fig. 5.

A: visual example for step length and limb angle calculations (far left) and example limb angles plotted as a function of time to demonstrate how spatial (e.g., center of oscillation difference) and temporal (e.g., phasing) gait parameters change from early adaptation (top) to late adaptation (bottom). Middle left shows a spatial shift, and middle right shows a temporal shift, with the gray lines indicating the original limb angle traces shown in the top diagram and the black lines indicating the limb angle traces after either a spatial (left) or temporal (right) shift. Black and white circles indicate the limb angles at slow leg heel strike and fast leg heel strike, respectively. Black and white arrows represent angular spread at heel strike of the slow and fast leg, which is analogous to step length. Note how the relative asymmetry in the size of the arrows during early adaptation is reduced by altering the spatial and temporal relationships between the 2 limbs. B: center of oscillation (top) and phasing (bottom) plotted against step length asymmetry during initial perturbation of adaptation 2. Pearson's correlation coefficients and corresponding P values are also presented for each comparison.

Fig. 6.

A: right belt speed data for each group during the fast and slow baseline recall tasks (curves show group mean ± SE). We did not observe differences among groups in the right belt speed selected during either baseline recall task. B: right belt speed data for each group across the entire time course of the split recall task. At the end of the task, we observed that the Gradual (black) and Extended Gradual (blue) groups selected significantly slower right belt speeds compared with the Abrupt (orange), Opposite Abrupt (red), and Short Abrupt (pink) groups (*P < 0.05). C: columns indicate the final right belt speeds selected during the split recall task for each group (mean ± SE). These data are equivalent to the data at the 10-min mark in B. Open circles show individual participant data. Note that all but 1 of the participants in the Gradual and Extended Gradual groups underestimated the target speed. *Significant difference from the Abrupt, Opposite Abrupt, and Short Abrupt groups with P < 0.05. D: Columns indicate the speed recall error during the split recall task for each group (mean ± SE). *Significant difference from the Abrupt, Opposite Abrupt, and Short Abrupt groups with P < 0.05; φtrend level difference from the Abrupt, Opposite Abrupt, and Short Abrupt groups with P = 0.06.