Changes in Muscle Synergy Structure and Activation Patterns Underlie Force Field Adaptation, Retention, and Generalization

Abstract

1Humans can adapt their motor commands in response to errors when they perform reaching movements in new dynamic conditions, a process called motor adaptation. They acquire knowledge about the new dynamics, which they can use when they are re-exposed and, limitedly, generalize to untrained reaching directions. While force field adaptation, retention, and generalization have been thoroughly investigated at a kinematic and kinetic task level, the underlying coordination at a muscular level remains unclear. Many studies propose that the central nervous system uses low- dimensional control, i.e., coordinates muscles in functional groups: so-called muscle synergies. Accordingly, we hypothesized that changes in muscle synergy structure and activation patterns represent the acquired knowledge underlying force field adaptation, retention, and generalization. To test this, 36 male humans practiced reaching to a single target in a viscous force field and were tested for retention and generalization to new directions, while we simultaneously measured muscle activity from 13 upper-body muscles. We found that muscle synergies used for unperturbed reaching cannot explain the muscle patterns when adapted. Instead, muscle synergies specific to this adapted state were necessary, alongside a novel four-phasic pattern of muscle synergy activation. Furthermore, these structural changes and patterns were also evident during retention and generalization. Our results suggest that reaching in an environment with altered dynamics requires structural changes to muscle synergies compared to unperturbed reaching, and that these changes facilitate retention and generalization. These findings provide new insights into how the central nervous system coordinates the muscles underlying motor adaptation, retention, and generalization. 2 Significance StatementHumans can adapt their reaching movements to new dynamic conditions. They acquire knowledge about the new dynamics and can use it not only when re-exposed to these conditions but also, in part, to generalize unpracticed reaching directions. While adaptation, retention, and generalization in a force field with new dynamics have been thoroughly investigated at a kinematic and kinetic task level, coordination of the underlying muscles remains elusive. Our results show how muscle synergies - functional groupings of co-activated muscles - underlie adaptation, retention, and generalization. In particular, we observed structural changes in the muscle synergies after adaptation compared to unperturbed reaching. These changes facilitate retention and spatial generalization. Thus, muscle synergies provide new insights into human motor adaptation.