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.

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.

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.

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.