Task-specific stability in muscle activation space during unintentional movements

Abstract

We used robot-generated perturbations applied during position-holding tasks to explore stability of induced unintentional movements in a multidimensional space of muscle activations. Healthy subjects held the handle of a robot against a constant bias force and were instructed not to interfere with hand movements produced by changes in the external force. Transient force changes were applied leading to handle displacement away from the initial position and then back toward the initial position. Intertrial variance in the space of muscle modes (eigenvectors in the muscle activations space) was quantified within two subspaces, corresponding to unchanged handle coordinate and to changes in the handle coordinate. Most variance was confined to the former subspace in each of the three phases of movement, the initial steady state, the intermediate position, and the final steady state. The same result was found when the changes in muscle activation were analyzed between the initial and final steady states. Changes in the dwell time between the perturbation force application and removal led to different final hand locations undershooting the initial position. The magnitude of the undershot scaled with the dwell time, while the structure of variance in the muscle activation space did not depend on the dwell time. We conclude that stability of the hand coordinate is ensured during both intentional and unintentional actions via similar mechanisms. Relative equifinality in the external space after transient perturbations may be associated with varying states in the redundant space of muscle activations. The results fit a hierarchical scheme for the control of voluntary movements with referent configurations and redundant mapping between the levels of the hierarchy.

Figure 1

The experimental setup, top view (top) and side view (bottom). The subject sat on a chair and grasped comfortably the handle of the robotic arm with the right hand. A sling supported the arm against the gravity. The robotic arm was aligned in such a way that the subject’s hand could move over 10 cm freely, mainly in a parasagittal plane along the negative X direction. Wireless active electrodes were used to record EMG signals from 10 muscles. The placement of a few electrodes is shown. LATR – lateral triceps; PDEL – posterior deltoid; LGTR – long head of triceps; ECRA – extensor carpi radialis.

Figure 2

Hand trajectories along the X-axis for a typical subject (Subject #3). The solid lines are the mean hand displacement along the X-axis across trials for the dwell times T_DWELL = 0 s (A), T_DWELL = 2 s (B), and T_DWELL = 5 s (C). The shaded areas show one standard error. Trials are aligned based on F_PERT onset (T₀). Preparation (before T₀) was the time period in which the subject held the handle in the initial position. During Perturbation (T₀ to T1), a change in the applied force took place (F_PERT≠ 0). Recovery (after T₁) represents the time interval following the removal of F_PERT. The dashed line at T₂ shows the end of the hand movement. SS₁, MID, and SS₂ are the time intervals selected for statistical analysis.

Figure 3

EMG traces for a subset of muscles, extensor carpi ulnaris (ECUL), flexor carpi ulnaris (FCUL), biceps (BICP), triceps long head (LGTR), posterior deltoid (PDEL), and latissimus dorsi (LATD) for a representative subject (Subject #2) with T_DWELL = 2 s. Averages across repetitive trials are presented; the shaded areas represent standard errors computed across trials. Muscle activations for each subject were normalized according to the averaged activity of the respective muscle during Position-holding trials (see Methods for details). The vertical dashed lines mark the start and the end of the perturbation force application.

Figure 4

Variance within the uncontrolled manifold, UCM (V_UCM) and within the orthogonal space (V_ORT) for the SS1, MID, and SS₂ phases and for the difference between the two steady states, ΔSS. Means ± SE across subjects are presented. The white, black, and striped bars show the data for T_DWELL = 0 s, 2 s, and 5 s conditions, respectively.

Figure 5

Fisher’s z-transformed synergy indices (ΔV_Z) for the SS1, MID, and SS₂ phases and for the difference between the two steady states, ΔSS. The bar plots show the mean values across subjects with standard error bars. The white, black, and striped bars show the data for T_DWELL = 0 s, 2 s, and 5 s conditions, respectively.

Figure 6

Within the suggested scheme, the task results in the creation of a referent configuration (RC_TASK) reflecting referent values for salient task-specific variables. RC_TASK projects on a redundant set of elemental referent configurations (RC_EL1; RC_E12; and RC_EL3) reflected in the structure of M-modes. Muscle activations in combination with the external forces result in changes in the actual body configurations, both AC_TASK and AC_EL. The difference between the RC and AC pairs drives changes in muscle activations until the system reaches an equilibrium state. The dashed line shows a hypothetical back-coupling process leading to drifts at the task level when the actual configuration is kept away from the corresponding RC for a relatively long time interval. Central back-coupling loops are not illustrated (see the text).