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.

Force matching: motor effects that are not reported by the actor.

We explored unintentional drifts of finger forces during force production and matching task. Based on earlier studies, we predicted that force matching with the other hand would reduce or stop the force drift in instructed fingers while uninstructed (enslaved) fingers remain unaffected. Twelve young, healthy, right-handed participants performed two types of tasks with both hands (task hand and match hand). The task hand produced constant force at 20% of MVC level with the Index and Ring fingers pressing in parallel on strain gauge force sensors. The Middle finger force wasn't instructed, and its enslaved force was recorded. Visual feedback on the total force by the instructed fingers was either present throughout the trial or only during the first 5 s (no-feedback condition). The other hand matched the perceived force level of the task hand starting at either 4, 8, or 15 s from the trial initiation. No feedback was ever provided for the match hand force. After the visual feedback was removed, the task hand showed a consistent drift to lower magnitudes of total force. Contrary to our prediction, over all conditions, force matching caused a brief acceleration of force drift in the task hand, which then reached a plateau. There was no effect of matching on drifts in enslaved finger force. We interpret the force drifts within the theory of control with spatial referent coordinates as consequences of drifts in the command (referent coordinate) to the antagonist muscles. This command is not adequately incorporated into force perception.

Motor unit-based synergies in a non-compartmentalized muscle.

The concept of synergies has been used to address the grouping of motor elements contributing to a task with the covariation of these elements reflecting task stability. This concept has recently been extended to groups of motor units with parallel scaling of the firing frequencies with possible contributions of intermittent recruitment (MU-modes) in compartmentalized flexor and extensor muscles of the forearm stabilizing force magnitude in finger pressing tasks. Here, we directly test for the presence and behavior of MU-modes in the tibialis anterior, a non-compartmentalized muscle. Ten participants performed an isometric cyclical dorsiflexion force production task at 1 Hz between 20 and 40% of maximal voluntary contraction and electromyographic (EMG) data were collected from two high-density wireless sensors placed on the skin over the right tibialis anterior. EMG data were decomposed into individual motor unit frequencies and resolved into sets of MU-modes. Inter-cycle analysis of MU-mode magnitudes within the framework of the uncontrolled manifold (UCM) hypothesis was used to quantify force-stabilizing synergies. Two or three MU-modes were identified in all participants and trials accounting, on average, for 69% of variance and were robust to cross-validation measurements. Strong dorsiflexion force-stabilizing synergies in the space of MU-modes were present in all participants and for both electrode locations as reflected in variance within the UCM (median 954, IQR 511-1924) exceeding variance orthogonal to the UCM (median 5.82, IQR 2.9-17.4) by two orders of magnitude. In contrast, MU-mode-stabilizing synergies in the space of motor unit frequencies were not present. This study offers strong evidence for the existence of synergic control mechanisms at the level of motor units independent of muscle compartmentalization, likely organized within spinal cord circuitry.

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.

Intramuscle Synergies: Their Place in the Neural Control Hierarchy.

We accept a definition of synergy introduced by Nikolai Bernstein and develop it for various actions, from those involving the whole body to those involving a single muscle. Furthermore, we use two major theoretical developments in the field of motor control-the idea of hierarchical control with spatial referent coordinates and the uncontrolled manifold hypothesis-to discuss recent studies of synergies within spaces of individual motor units (MUs) recorded within a single muscle. During the accurate finger force production tasks, MUs within hand extrinsic muscles form robust groups, with parallel scaling of the firing frequencies. The loading factors at individual MUs within each of the two main groups link them to the reciprocal and coactivation commands. Furthermore, groups are recruited in a task-specific way with gains that covary to stabilize muscle force. Such force-stabilizing synergies are seen in MUs recorded in the agonist and antagonist muscles but not in the spaces of MUs combined over the two muscles. These observations reflect inherent trade-offs between synergies at different levels of a control hierarchy. MU-based synergies do not show effects of hand dominance, whereas such effects are seen in multifinger synergies. Involuntary, reflex-based, force changes are stabilized by intramuscle synergies but not by multifinger synergies. These observations suggest that multifinger (multimuscle synergies) are based primarily on supraspinal circuitry, whereas intramuscle synergies reflect spinal circuitry. Studies of intra- and multimuscle synergies promise a powerful tool for exploring changes in spinal and supraspinal circuitry across patient populations.

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.