Reduction of metabolic cost during motor learning of arm reaching dynamics

Abstract

It is often assumed that the CNS controls movements in a manner that minimizes energetic cost. While empirical evidence for actual metabolic minimization exists in locomotion, actual metabolic cost has yet to be measured during motor learning and/or arm reaching. Here, we measured metabolic power consumption using expired gas analysis, as humans learned novel arm reaching dynamics. We hypothesized that (1) metabolic power would decrease with motor learning and (2) muscle activity and coactivation would parallel changes in metabolic power. Seated subjects made horizontal planar reaching movements toward a target using a robotic arm. The novel dynamics involved compensating for a viscous curl force field that perturbed reaching movements. Metabolic power was measured continuously throughout the protocol. Subjects decreased movement error and learned the novel dynamics. By the end of learning, net metabolic power decreased by ~20% (~0.1 W/kg) from initial learning. Muscle activity and coactivation also decreased with motor learning. Interestingly, distinct and significant reductions in metabolic power occurred even after muscle activity and coactivation had stabilized and movement changes were small. These results provide the first evidence of actual metabolic reduction during motor learning and for a reaching task. Further, they suggest that muscle activity may not explain changes in metabolic cost as completely as previously thought. Additional mechanisms such as more subtle features of arm muscle activity, changes in activity of other muscles, and/or more efficient neural processes may also underlie the reduction in metabolic cost during motor learning.

Figures

Figure 1.

Experiment setup and force fields: A, Subjects made horizontal planar reaching movements using a robotic arm, while breathing through a mouthpiece to measure rates of oxygen consumption and carbon dioxide production. The subject's arm was supported in a cradle attached to the robot handle. Odd numbered trials involved reaching outwards to the target while even trials involved reaching inwards. An auditory metronome paced subjects to start movements at 2 s intervals. B, Schematic of the viscous curl force field. On outward movements, the force field applied a perturbation to the left (−x) and for inward movements, the perturbation was to the right (+x). C, Schematic of the force channel used during the catch trials to measure the anticipatory force subjects planned to use to counter the perturbing force of the curl force field.

Figure 2.

Experimental protocol and example of data hierarchy. There were 6 blocks: baseline resting (light gray), Null 1 (gray), Force 1 (bold gray), Force 2 (bold black), Null 2 (gray), and postresting (light gray). Colors are used in other figures to associate data with specific blocks. During the Force 1 and Force 2 blocks, subjects made reaching movements in the curl force field. All metrics were calculated early and late in each reaching block (Null 1, Force 1, Force 2, and Null 2). Pmet, metabolic power. Trial attributes for late Force 1 are provided as an example of the data hierarchy. A batch consisted of five trials. One trial within each batch was a catch trial. Electromyographic data (EMG) were collected for every odd numbered trial.

Figure 3.

Time courses of movement error (A), anticipatory force (B), net metabolic power (C), and RMS EMG and RMS coactivation (D) by batches throughout the protocol. Lines are group means, and shaded areas depict ±SEM. The dotted vertical lines in A outline that the overall learning period spans from early Force 1 to late Force 2, that fast learning occurs from early Force 1 to late Force 1, and that slow learning occurs from late Force 1 to late Force 2. The dark gray horizontal thin line in net metabolic power (C) represents the average for the last 2 min of Force 1. This highlights that net metabolic power output during late Force 2 was less than during late Force 1. Muscles and muscle pairs had similar time courses so only the shoulder muscle pair (pectoralis major and posterior deltoid) is shown. N = 7 for EMG data and N = 15 for all other measures. EMG and coactivation data were normalized by task to late Null 1 and are reported as arbitrary units (a.u.).

Figure 4.

Changes in movements and electromyography during overall motor learning in a representative subject. Overall motor learning occurred from early Force 1 (gray) to late Force 2 (black). Traces are the mean for the odd numbered trials (outward movements) in early Force 1 and late Force 2. A, The movement path at early Force 1 had a large movement error compared with the straight line path at late Force 2. B, The y-velocity profile at early Force 1 was biphasic compared with the bell-shaped profile at late Force 2. C, Anticipatory force increased from early Force 1 to late Force 2. D, Muscle activity and coactivation was greater at early Force 1 compared with late Force 2. EMG and coactivation data were normalized by task to late Null 1 and are reported as arbitrary units (a.u.).

Figure 5.

Group averaged data for movement error (A), anticipatory force (B), net metabolic power (C), and RMS EMG and RMS coactivation (D) during overall, fast, and slow motor learning. During overall motor learning from early Force 1 to late Force 2, movement error, net metabolic power, RMS EMG of the posterior deltoid, and RMS coactivation of the pectoralis major-posterior deltoid pair decreased significantly and anticipatory force also increased significantly. During fast motor learning, early Force 1 to late Force 1, all metrics except net metabolic power had significant changes. During slow motor learning, late Force 1 to late Force 2, net metabolic power decreased significantly as movement error and anticipatory force also improved significantly, though small in amplitude. Muscles and muscle pairs had similar trends so only the shoulder muscle pair (pectoralis major and posterior deltoid) is shown. Error bars indicate SEM. P values are for paired t tests of planned comparisons. N = 7 for EMG data and N = 15 for all other measures. EMG and coactivation data were normalized by task to late Null 1 and are reported as arbitrary units (a.u.).

Figure 6.

Fine-tuning of movements and electromyography during slow motor learning in a representative subject. Slow motor learning was from late Force 1 (gray) to late Force 2 (black). Late Null 1 (thin gray) is plotted as a reference of baseline movements. Traces are the mean for the odd numbered trials (outward movements) in late Null 1, late Force 1, and late Force 2. A, Movement paths for late Null 1, late Force 1, and late Force 2 were relatively straight. Movement error data of movement paths at late Force 2 were less than late Force 1, indicating that fine-tuning was ongoing. B, The y-velocity profiles had similar magnitudes and bell-shaped profiles. C, The magnitude of anticipatory force for late Force 2 was greater than late Force 1, suggesting that motor learning was still occurring. An anticipatory force profile for Null 1 was not included because anticipatory forces during Null 1 were negligible. D, Muscle activity and coactivation were similar during late Null 1, late Force 1, and late Force 2. Less muscle activity was observed during late Null 1 compared with late Force 1 or late Force 2 because there was no curl force field to counter during null trials. EMG and coactivation data were normalized by task to late Null 1 and are reported as arbitrary units (a.u.).

Figure 7.

Reduction in net metabolic power consumption during slow motor learning in all individual subjects. When movements and muscle activity were being fine-tuned, group averaged net metabolic power consumption still decreased significantly by 14% from late Force 1 to late Force 2 (0.50 ± 0.05 W/kg vs 0.43 ± 0.05 W/kg). This metabolic reduction was consistent among subjects. Thirteen of 15 subjects (solid lines) reduced net metabolic power from late Force 1 to late Force 2, whereas only two subjects (dashed lines) increased net metabolic power. Net metabolic power of late Null 1 and late Null 2 were not significantly different (p = 0.7726). Error bars indicate SEM. P values are paired t tests of planned comparisons.