Muscle synergies for multidirectional isometric force generation during maintenance of upright standing posture.

Muscle synergies are defined as coordinated recruitment of groups of muscles with specific activation balances and time profiles aimed at generating task-specific motor commands. While muscle synergies in postural control have been investigated primarily in reactive balance conditions, the neuromechanical contribution of muscle synergies during voluntary control of upright standing is still unclear. In this study, muscle synergies were investigated during the generation of isometric force at the trunk during the maintenance of standing posture. Participants were asked to maintain the steady-state upright standing posture while pulling forces of different magnitudes were applied at the level at the waist in eight horizontal directions. Muscle synergies were extracted by nonnegative matrix factorization from sixteen lower limb and trunk muscles. An average of 5-6 muscle synergies were sufficient to account for a wide variety of EMG waveforms associated with changes in the magnitude and direction of pulling forces. A cluster analysis partitioned the muscle synergies of the participants into a large group of clusters according to their similarity, indicating the use of a subjective combination of muscles to generate a multidirectional force vector in standing. Furthermore, we found a participant-specific distribution in the values of cosine directional tuning parameters of synergy amplitude coefficients, suggesting the existence of individual neuromechanical strategies to stabilize the whole-body posture. Our findings provide a starting point for the development of novel diagnostic tools to assess muscle coordination in postural control and lay the foundation for potential applications of muscle synergies in rehabilitation.

Three Levels of Neural Control Contributing to Performance-stabilizing Synergies in Multi-finger Tasks.

We tested a hypothesis on force-stabilizing synergies during four-finger accurate force production at three levels: (1) The level of the reciprocal and coactivation commands, estimated as the referent coordinate and apparent stiffness of all four fingers combined; (2) The level of individual finger forces; and (3) The level of firing of individual motor units (MU). Young, healthy participants performed accurate four-finger force production at a comfortable, non-fatiguing level under visual feedback on the total force magnitude. Mechanical reflections of the reciprocal and coactivation commands were estimated using small, smooth finger perturbations applied by the "inverse piano" device. Firing frequencies of motor units in the flexor digitorum superficialis (FDS) and extensor digitorum communis (EDC) were estimated using surface recording. Principal component analysis was used to identify robust MU groups (MU-modes) with parallel changes in the firing frequency. The framework of the uncontrolled manifold hypothesis was used to compute synergy indices in the spaces of referent coordinate and apparent stiffness, finger forces, and MU-mode magnitudes. Force-stabilizing synergies were seen at all three levels. They were present in the MU-mode spaces defined for MUs in FDS, in EDC, and pooled over both muscles. No effects of hand dominance were seen. The synergy indices defined at different levels of analysis showed no correlations across the participants. The findings are interpreted within the theory of control with spatial referent coordinates for the effectors. We conclude that force stabilization gets contributions from three levels of neural control, likely associated with cortical, subcortical, and spinal circuitry.

Two classes of action-stabilizing synergies reflecting spinal and supraspinal circuitry.

We explored force-stabilizing synergies during accurate four-finger constant force production tasks in spaces of finger modes (commands to fingers computed to account for the finger interdependence) and of motor unit (MU) firing frequencies. The main specific hypothesis was that the multifinger synergies would disappear during unintentional force drifts without visual feedback on the force magnitude, whereas MU-based synergies would be robust to such drifts. Healthy participants performed four-finger accurate cyclical force production trials followed by trials of constant force production. Individual MUs were identified in the flexor digitorum superficialis (FDS) and extensor digitorum communis (EDC). Principal component analysis was applied to motor unit frequencies to identify robust MU groups (MU-modes) with parallel scaling of the firing frequencies in FDS, in EDC, and the combined MUs of FDS + EDC. The framework of the uncontrolled manifold hypothesis was used to quantify force-stabilizing synergies when visual feedback on the force magnitude was available and 15 s after turning the visual feedback off. Removing visual feedback led to a force drift toward lower magnitudes, accompanied by the disappearance of multifinger synergies. In contrast, MU-mode synergies were minimally affected by removing visual feedback off and continued to be robust for the FDS and for the EDC, while being absent for the (FDS + EDC) analysis. We interpret the findings within the theory of hierarchical control of action with spatial referent coordinates. The qualitatively different behavior of the multifinger and MU-mode-based synergies likely reflects the difference in the involved neural circuitry, supraspinal for the former and spinal for the latter.NEW & NOTEWORTHY Two types of synergies, in the space of commands to individual fingers and in the space of motor unit groups, show qualitatively different behaviors during accurate multifinger force-production tasks. After removing visual feedback, finger force synergies disappear, whereas motor unit-based synergies persist. These results point at different neural circuitry involved in these two basic classes of synergies: supraspinal for multieffector synergies, and spinal for motor unit-based synergies.

Effects of fatigue on intramuscle force-stabilizing synergies.

We applied the recently introduced concept of intramuscle synergies in spaces of motor units (MUs) to quantify indexes of such synergies in the tibialis anterior during ankle dorsiflexion force production tasks and their changes with fatigue. We hypothesized that MUs would be organized into robust groups (MU modes), which would covary across trials to stabilize force magnitude, and the indexes of such synergies would drop under fatigue. Healthy, young subjects (n = 15; 8 females) produced cyclical, isometric dorsiflexion forces while surface electromyography was used to identify action potentials of individual MUs. Principal component analysis was used to define MU modes. The framework of the uncontrolled manifold (UCM) was used to analyze intercycle variance and compute the synergy index, ΔVZ. Cyclical force production tasks were repeated after a nonfatiguing exercise (control) and a fatiguing exercise. Across subjects, fatigue led, on average, to a 43% drop in maximal force and fewer identified MUs per subject (29.6 ± 2.1 vs. 32.4 ± 2.1). The first two MU modes accounted for 81.2 ± 0.08% of variance across conditions. Force-stabilizing synergies were present across all conditions and were diminished after fatiguing exercise (1.49 ± 0.40) but not control exercise (1.76 ± 0.75). Decreased stability after fatigue was caused by an increase in the amount of variance orthogonal to the UCM. These findings contrast with earlier studies of multieffector synergies demonstrating increased synergy index under fatigue. We interpret the results as reflections of a drop in the gain of spinal reflex loops under fatigue. The findings corroborate an earlier hypothesis on the spinal nature of intramuscle synergies.NEW & NOTEWORTHY Across multielement force production tasks, fatigue of an element leads to increased indexes of force stability (synergy indexes). Here, however, we show that groups of motor units in the tibialis anterior show decreased indexes of force-stabilizing synergies after fatiguing exercise. These findings align intramuscle synergies with spinal mechanisms, in contrast to the supraspinal control of multimuscle synergies.