Rapid feedback responses correlate with reach adaptation and properties of novel upper limb loads

Abstract

A hallmark of voluntary motor control is the ability to adjust motor patterns for novel mechanical or visuomotor contexts. Recent work has also highlighted the importance of feedback for voluntary control, leading to the hypothesis that feedback responses should adapt when we learn new motor skills. We tested this prediction with a novel paradigm requiring that human subjects adapt to a viscous elbow load while reaching to three targets. Target 1 required combined shoulder and elbow motion, target 2 required only elbow motion, and target 3 (probe target) required shoulder but no elbow motion. This simple approach controlled muscle activity at the probe target before, during, and after the application of novel elbow loads. Our paradigm allowed us to perturb the elbow during reaching movements to the probe target and identify several key properties of adapted stretch responses. Adapted long-latency responses expressed (de-) adaptation similar to reaching errors observed when we introduced (removed) the elbow load. Moreover, reaching errors during learning correlated with changes in the long-latency response, showing subjects who adapted more to the elbow load displayed greater modulation of their stretch responses. These adapted responses were sensitive to the size and direction of the viscous training load. Our results highlight an important link between the adaptation of feedforward and feedback control and suggest a key part of motor adaptation is to adjust feedback responses to the requirements of novel motor skills.

Figure 1.

Experimental apparatus and learning patterns. A, Experimental setup and target configuration. Red arrow denotes the viscous elbow load applied during reaching movements in the adaptation block. Subjects reached to targets configured in a joint-based coordinate system (T1–T3). B, Representative hand paths obtained from a single subject during training. Black, red, and blue traces correspond to baseline, adaptation, and washout phases. Thick lines are the first trial, thin lines the last trial in each respective block. C, Trial-by-trial changes in maximum perpendicular error at each target (mean ± SEM). Positive values denote counterclockwise rotation of the hand from the target (elbow flexion is positive). Light shaded region corresponds to the adaptation period when the novel elbow load was applied. D, Reaching errors observed at each target (mean ± SEM). Black, red, and blue bars correspond to the mean of the maximum perpendicular errors in the baseline (BL), early adaptation (EA), late adaptation (LA), and washout (WO) phases, respectively. *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 2.

Muscle activity and integrated EMG. A, EMG activity of four monoarticular arm muscles is shown for each reaching target during the baseline (black trace), adaptation (red trace), and washout phases (blue trace). Horizontal axis is the time relative to reach onset (dashed vertical line) and the vertical axis is normalized muscle activity (a.u.). Due to the normalization process, 1 a.u. corresponds to the level of muscle activity needed to stabilize against a 1 Nm constant load. EMG data are aligned to movement onset (0 ms) and the shaded region indicates the SEM. For display purposes, the EMG was smoothed using a 10 sample (10 ms) moving-average. B, Integrated EMG activity for the pair of antagonist muscles spanning the elbow and shoulder joints at each target. All values were obtained from the 300 ms window before movement onset. *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 3.

Comparison of kinematic responses evoked by mechanical perturbations. A, Exemplar data from a single subject showing corrective responses elicited by a mechanical perturbation. Black, red, and blue traces correspond to average responses obtained during the baseline, late adaptation, and washout phases. Dashed lines are the average from unperturbed reaching movements in each phase of the experiment; solid lines are the average from perturbation trials. Diagonal tick marks are the hand position every 100 ms. B, Perturbation-evoked hand motion (mean ± SEM). Data are plotted in the same format as in A. C, Temporal kinematics of the elbow joint. Data aligned to perturbation onset (t = 0 ms; mean ± SEM). D, Same format as B, but for elbow reversal angles. *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 4.

Muscle stretch responses across the adaptation paradigm. A, Perturbation responses of the brachioradialis (left) and triceps lateral (right) muscles (mean ± SEM). Black, red, and blue traces correspond to brachioradialis stretch responses in the baseline, adaptation, and washout phases. Data are aligned to perturbation onset (t = 0 ms) and dashed vertical lines separate the different time phases of the stretch response. B, Pectoralis major and posterior deltoid stretch responses. Data are plotted in the same format as in B. C, Coactivation ratio between triceps lateral and brachioradialis during each phase of the stretch response. Color scheme is the same as in A and B. D, Coactivation ratio between pectoralis major and posterior deltoid stretch responses. Color scheme is the same as in C.

Figure 5.

Magnitude of brachioradialis stretch responses and relation to adaptation of voluntary reaching behavior. A, Binned analysis of brachioradialis stretch responses (mean ± SEM). Black, red, and blue bars correspond to brachioradialis stretch responses in the baseline, late adaptation, and washout phases. B, Trial-by-trial adaptation of muscle activity in the long-latency time period (mean ± SEM). C, Correlates of reach adaptation in feedback responses. Vertical axis is change in LL responses between baseline and late adaptation phase. Horizontal axis shows individual subjects' perpendicular errors averaged across the training targets (T1 and T2) for the late adaptation phase. *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 6.

Corrective responses for different perturbation schedules. A, Schematic showing the order of perturbation trials in fixed (unperturbed trials randomized, perturbation trials inserted on every eighth reaching trial; top, red arrows) and random trial blocks (unperturbed and perturbed reaching trials randomized; bottom, blue arrows). B, Exemplar data from a single subject showing corrective responses elicited by a mechanical perturbation. Black, red, and blue traces correspond to average responses obtained during the baseline, late adaptation, and washout phases. Diagonal tick marks correspond to the hand position every 100 ms. C, Population-level elbow joint kinematics evoked by mechanical probe trials. Data are aligned to perturbation onset (t = 0 ms; mean ± SEM). Negative changes in elbow angles represent extension motion caused by the perturbation. D, Population averages showing perturbation responses of the brachioradialis muscle (mean ± SEM). Red and blue traces correspond to brachioradialis responses in the pseudorandom and random trial blocks. E, Binned analysis of brachioradialis perturbation responses (mean ± SEM). *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 7.

LL responses express knowledge of the viscosity of novel elbow-joint loads. A, Experimental apparatus and target configuration. Red (1 Nm·s/rad) and blue (2 Nm·s/rad) arrows represent the viscous elbow load in the adaptation block. B, Exemplar data showing corrective responses across the paradigm. Black, red, and blue traces correspond to unloaded reaching, 1 Nm·s/rad viscous elbow load, and 2 Nm·s/rad viscous elbow load. Dashed lines are the average unperturbed reaching movements in each phase of the experiment; solid lines are the average movement in perturbation trials. Diagonal tick marks correspond to the hand position every 100 ms. C, Summary plot showing perturbation-evoked hand motion in each phase of the adaptation paradigm (mean ± SEM). D, Mean perturbation-evoked activity of the brachioradialis muscle (N = 20). The dashed lines demarcate the binned epochs used to characterize muscle stretch responses. Horizontal axis is the time relative to perturbation onset (solid vertical line; t = 0 ms). The shaded region indicates the SEM with the same color scheme as in B. E, Binned analysis of muscle stretch responses (mean ± SEM). Color scheme is the same as in B. *p < 0.05, **P < 0.01, ***p < 0.001.

Figure 8.

Adaptation of LL responses is sensitive to the direction of the training load. A, Representative data from a single subject showing corrective responses across the training paradigm with the brachioradialis muscle preloaded. Black trace corresponds to trajectories during unloaded reaching (baseline); red traces are trajectories from the adaptation phase (viscous elbow load). Solid lines correspond to probe trials (± 2 Nm step-torque perturbation) and the dashed lines represent unperturbed trajectories. B, Summary plot showing maximum perpendicular hand motion (mean ± SEM) caused by perturbations that extended (left) or flexed (right) the elbow. C, Brachioradialis stretch responses evoked by elbow extensor perturbations. Left panel: Mean perturbation-evoked activity of the brachioradialis muscle for mechanical perturbations that extended the elbow. Vertical dashed lines demarcate the time epochs used to characterize muscle stretch responses. Horizontal axis is the time relative to perturbation onset (t = 0 ms; solid vertical line). Shaded regions indicate the SEM with black and red shading corresponding to brachioradialis activity in the baseline and adaptation phases, respectively. Right, Binned analysis of brachioradialis stretch responses for perturbations that extended the elbow. D, Triceps lateral stretch responses evoked by elbow extensor perturbations. Left, Mean perturbation-evoked activity of the triceps lateral muscle for extensor perturbations. Data are plotted in the same format as in C, Right, Binned analysis of triceps lateral stretch responses for perturbations that extended the elbow. E, Brachioradialis stretch responses evoked by elbow flexor perturbations. Left, Mean perturbation-evoked activity of the brachioradialis muscle for perturbations that flexed the elbow. F, Triceps lateral stretch responses evoked by perturbations that flexed the elbow. Left, Mean perturbation-evoked activity of the triceps lateral muscle. Right, Binned analysis of triceps lateral responses. Data are plotted in the same format as panel C. *p < 0.05, **P < 0.01, ***p < 0.001.

Figure 9.

LL responses with the adapted muscle preinhibited are sensitive to the direction of the training load. A, Brachioradialis stretch responses evoked by elbow extensor perturbations. Left, Mean perturbation-evoked activity of the preinhibited brachioradialis muscle for mechanical perturbations that extended the elbow. Vertical dashed lines demarcate the time epochs used to characterize muscle feedback responses. Horizontal axis is the time relative to perturbation onset (t = 0 ms; solid vertical line). Shaded regions indicate the SEM with black and red shading corresponding to brachioradialis activity in the baseline and adaptation phases, respectively. Right, Binned analysis of brachioradialis stretch responses for perturbations that extended the elbow. B, Stretch responses for the preloaded triceps lateral muscle evoked by elbow extensor perturbations. Left, Mean perturbation-evoked activity of the triceps lateral muscle for extensor perturbations. Data are plotted in the same format and color scheme as in A. Right, Binned analysis of triceps lateral stretch responses for perturbations that extended the elbow. C, Brachioradialis stretch responses evoked by elbow flexor perturbations. Left, Mean perturbation-evoked activity of the brachioradialis muscle for perturbations that flexed the elbow. D, Triceps lateral stretch responses evoked by perturbations that flexed the elbow. Left, Mean perturbation-evoked activity of the triceps lateral muscle. Right, Binned analysis of triceps lateral responses. Data are plotted in the same format and color scheme as panel A. *p < 0.05, **P < 0.01, ***p < 0.001.