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

Abstract

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.