Exposure to an incompatible virtual surgery impacts the null space components of the muscle patterns after re-adaptation but not the task performance.

Under the synergy hypothesis, novel muscle synergies may be required for motor skill learning. We have developed a "virtual surgery" experimental paradigm that alters the mapping of muscle activations onto virtual cursor motion during an isometric reaching task using myoelectric control. By creating virtual surgeries that are "incompatible" with the original synergies, we can investigate learning new muscle synergies in controlled experimental conditions. We have previously shown that participants are able to improve their task performance after an incompatible virtual surgery, using novel muscle patterns to overcome the perturbation. In this work, we investigated whether the activation of novel muscle patterns, that are required after an incompatible virtual surgery, affects task performance or the muscle patterns after re-adaptation to the unperturbed baseline mapping. We found that experiencing an incompatible virtual surgery did not affect the task performance during the baseline mapping. However, the adaptation to the incompatible virtual surgery resulted in changes in the null space components of the muscle patterns used in the unperturbed task.

A novel force-constrained non-negative matrix factorization algorithm reveals the effectiveness of muscle synergies in the task space.

According to the synergy hypothesis, the motor system recruits a small number of synergies in a task-dependent manner. Existing synergy extraction algorithms typically only consider the muscle pattern and it remains unclear to which extent muscle synergies encode task-relevant variations of muscle activity. We propose a novel force-constrained non-negative matrix algorithm (FCNMF) based on a gradient descent update rule that considers also the task space by adding a term penalizing force reconstruction error in the cost function. We validated the FCNMF algorithm using simulated muscle data and corrupted them by noise. We compared task performances with reconstructed trajectories using synergies (RS) extracted from the FCNMF algorithm and from the standard multiplicative non-negative matrix factorization NMF algorithm. We found that FCNMF outperforms NMF for different types of noise. Finally, we demonstrated the effectiveness of FCNMF on EMG data collected during an isometric reaching task. The new algorithm accurately reconstructs the trajectories in all participants, even in those for which the NMF algorithm fails. These findings show the effectiveness of muscle synergies extracted considering the task space, possibly thanks to the robustness of FCNMF against non-isotropic noise present in muscle data, suggesting that they provide an effective strategy for motor coordination.

Persistent changes in motor adaptation strategies after perturbations that require exploration of novel muscle activation patterns.

Motor skill learning requires the acquisition of novel muscle patterns and a new control policy-a process that requires time. In contrast, motor adaptation often requires only the adjustment of existing muscle patterns-a fast process. By altering the mapping of muscle activations onto cursor movements in a myoelectrically controlled virtual environment, we are able to create perturbations that require either the recombination of existing muscle synergies (compatible virtual surgery) or the learning of novel muscle patterns (incompatible virtual surgery). We investigated whether adaptation to a compatible surgery is affected by prior exposure to an incompatible surgery, i.e., a motor skill learning task. We found that adaptation to a compatible surgery was characterized by a decrease in the quality of muscle pattern reconstructions using the original synergies and an increase in reaction times only after exposure to an incompatible surgery. In contrast, prior exposure to a compatible surgery did not affect the learning process required to overcome an incompatible surgery. The fact that exposure to an incompatible surgery had a profound effect on the muscle patterns during the adaptation to a subsequent compatible surgery and not vice versa suggests that null space exploration, possibly combined with an explicit exploration strategy, is engaged during exposure to an incompatible surgery and remains enhanced during a new adaptation episode. We conclude that motor skill learning, requiring novel muscle activation patterns, leads to changes in the exploration strategy employed during a subsequent perturbation.NEW & NOTEWORTHY Motor skill learning requires the acquisition of novel muscle patterns, whereas motor adaptation requires adjusting existing ones. We wondered whether training a new motor skill affects motor adaptation strategies. We show that learning an incompatible perturbation, a complex skill requiring new muscle synergies, affects the muscle patterns observed during adaption to a compatible perturbation, which requires adjusting the existing synergies. Our results suggest that motor skill learning results in persistent changes in the exploration strategy.

Task space exploration improves adaptation after incompatible virtual surgeries.

Humans have a remarkable capacity to learn new motor skills, a process that requires novel muscle activity patterns. Muscle synergies may simplify the generation of muscle patterns through the selection of a small number of synergy combinations. Learning of new motor skills may then be achieved by acquiring novel muscle synergies. In a previous study, we used myoelectric control to construct virtual surgeries that altered the mapping from muscle activity to cursor movements. After compatible virtual surgeries, which could be compensated by recombining subject-specific muscle synergies, participants adapted quickly. In contrast, after incompatible virtual surgeries, which could not be compensated by recombining existing synergies, participants explored new muscle patterns but failed to adapt. Here, we tested whether task space exploration can promote learning of novel muscle synergies required to overcome an incompatible surgery. Participants performed the same reaching task as in our previous study but with more time to complete each trial, thus allowing for exploration. We found an improvement in trial success after incompatible virtual surgeries. Remarkably, improvements in movement direction accuracy after incompatible surgeries occurred faster for corrective movements than for the initial movement, suggesting that learning of new synergies is more effective when used for feedback control. Moreover, reaction time was significantly higher after incompatible than compatible virtual surgeries, suggesting an increased use of an explicit adaptive strategy to overcome incompatible surgeries. Taken together, these results indicate that exploration is important for skill learning and suggest that human participants, with sufficient time, can learn new muscle synergies.NEW & NOTEWORTHY Motor skill learning requires the acquisition of novel muscle patterns, a slow adaptive process. Here we show that learning to control a cursor after an incompatible virtual surgery, a complex skill requiring new muscle synergies, is possible when enough time for task space exploration is provided. Our results suggest that learning new synergies is related to the exceptional human capacity to acquire a wide variety of novel motor skills with practice.

Can spatial filtering separate voluntary and involuntary components in children with dyskinetic cerebral palsy?

The design of myocontrolled devices faces particular challenges in children with dyskinetic cerebral palsy because the electromyographic signal for control contains both voluntary and involuntary components. We hypothesized that voluntary and involuntary components of movements would be uncorrelated and thus detectable as different synergistic patterns of muscle activity, and that removal of the involuntary components would improve online EMG-based control. Therefore, we performed a synergy-based decomposition of EMG-guided movements, and evaluated which components were most controllable using a Fitts' Law task. Similarly, we also tested which muscles were most controllable. We then tested whether removing the uncontrollable components or muscles improved overall function in terms of movement time, success rate, and throughput. We found that removal of less controllable components or muscles did not improve EMG control performance, and in many cases worsened performance. These results suggest that abnormal movement in dyskinetic CP is consistent with a pervasive distortion of voluntary movement rather than a superposition of separable voluntary and involuntary components of movement.

Does the cerebellum shape the spatiotemporal organization of muscle patterns? Insights from subjects with cerebellar ataxias.

The role of the cerebellum in motor control has been investigated extensively, but its contribution to the muscle pattern organization underlying goal-directed movements is still not fully understood. Muscle synergies may be used to characterize multimuscle pattern organization irrespective of time (spatial synergies), in time irrespective of the muscles (temporal synergies), and both across muscles and in time (spatiotemporal synergies). The decomposition of muscle patterns as combinations of different types of muscle synergies offers the possibility to identify specific changes due to neurological lesions. In this study, we recorded electromyographic activity from 13 shoulder and arm muscles in subjects with cerebellar ataxias (CA) and in age-matched healthy subjects (HS) while they performed reaching movements in multiple directions. We assessed whether cerebellar damage affects the organization of muscle patterns by extracting different types of muscle synergies from the muscle patterns of each HS and using these synergies to reconstruct the muscle patterns of all other participants. We found that CA muscle patterns could be accurately captured only by spatial muscle synergies of HS. In contrast, there were significant differences in the reconstruction R2 values for both spatiotemporal and temporal synergies, with an interaction between the two synergy types indicating a larger difference for spatiotemporal synergies. Moreover, the reconstruction quality using spatiotemporal synergies correlated with the severity of impairment. These results indicate that cerebellar damage affects the temporal and spatiotemporal organization, but not the spatial organization, of the muscle patterns, suggesting that the cerebellum plays a key role in shaping their spatiotemporal organization.NEW & NOTEWORTHY In recent studies, the decomposition of muscle activity patterns has revealed a modular organization of the motor commands. We show, for the first time, that muscle patterns of subjects with cerebellar damage share with healthy controls spatial, but not temporal and spatiotemporal, modules. Moreover, changes in spatiotemporal organization characterize the severity of the subject's impairment. These results suggest that the cerebellum has a specific role in shaping the spatiotemporal organization of the muscle patterns.

Muscle patterns underlying voluntary modulation of co-contraction.

Manipulative actions involving unstable interactions with the environment require controlling mechanical impedance through muscle co-contraction. While much research has focused on how the central nervous system (CNS) selects the muscle patterns underlying a desired movement or end-point force, the coordination strategies used to achieve a desired end-point impedance have received considerably less attention. We recorded isometric forces at the hand and electromyographic (EMG) signals in subjects performing a reaching task with an external disturbance. In a virtual environment, subjects displaced a cursor by applying isometric forces and were instructed to reach targets in 20 spatial locations. The motion of the cursor was then perturbed by disturbances whose effects could be attenuated by increasing co-contraction. All subjects could voluntarily modulate co-contraction when disturbances of different magnitudes were applied. For most muscles, activation was modulated by target direction according to a cosine tuning function with an offset and an amplitude increasing with disturbance magnitude. Co-contraction was characterized by projecting the muscle activation vector onto the null space of the EMG-to-force mapping. Even in the baseline the magnitude of the null space projection was larger than the minimum magnitude required for non-negative muscle activations. Moreover, the increase in co-contraction was not obtained by scaling the baseline null space projection, scaling the difference between the null space projections in any block and the projection of the non-negative minimum-norm muscle vector, or scaling the difference between the null space projections in the perturbed blocks and the baseline null space projection. However, the null space projections in the perturbed blocks were obtained by linear combination of the baseline null space projection and the muscle activation used to increase co-contraction without generating any force. The failure of scaling rules in explaining voluntary modulation of arm co-contraction suggests that muscle pattern generation may be constrained by muscle synergies.

Effective force control by muscle synergies.

Muscle synergies have been proposed as a way for the central nervous system (CNS) to simplify the generation of motor commands and they have been shown to explain a large fraction of the variation in the muscle patterns across a variety of conditions. However, whether human subjects are able to control forces and movements effectively with a small set of synergies has not been tested directly. Here we show that muscle synergies can be used to generate target forces in multiple directions with the same accuracy achieved using individual muscles. We recorded electromyographic (EMG) activity from 13 arm muscles and isometric hand forces during a force reaching task in a virtual environment. From these data we estimated the force associated to each muscle by linear regression and we identified muscle synergies by non-negative matrix factorization. We compared trajectories of a virtual mass displaced by the force estimated using the entire set of recorded EMGs to trajectories obtained using 4-5 muscle synergies. While trajectories were similar, when feedback was provided according to force estimated from recorded EMGs (EMG-control) on average trajectories generated with the synergies were less accurate. However, when feedback was provided according to recorded force (force-control) we did not find significant differences in initial angle error and endpoint error. We then tested whether synergies could be used as effectively as individual muscles to control cursor movement in the force reaching task by providing feedback according to force estimated from the projection of the recorded EMGs into synergy space (synergy-control). Human subjects were able to perform the task immediately after switching from force-control to EMG-control and synergy-control and we found no differences between initial movement direction errors and endpoint errors in all control modes. These results indicate that muscle synergies provide an effective strategy for motor coordination.

Differences in adaptation rates after virtual surgeries provide direct evidence for modularity.

Whether the nervous system relies on modularity to simplify acquisition and control of complex motor skills remains controversial. To date, evidence for modularity has been indirect, based on statistical regularities in the motor commands captured by muscle synergies. Here we provide direct evidence by testing the prediction that in a truly modular controller it must be harder to adapt to perturbations that are incompatible with the modules. We investigated a reaching task in which human subjects used myoelectric control to move a mass in a virtual environment. In this environment we could perturb the normal muscle-to-force mapping, as in a complex surgical rearrangement of the tendons, by altering the mapping between recorded muscle activity and simulated force applied on the mass. After identifying muscle synergies, we performed two types of virtual surgeries. After compatible virtual surgeries, a full range of movements could still be achieved recombining the synergies, whereas after incompatible virtual surgeries, new or modified synergies would be required. Adaptation rates after the two types of surgery were compared. If synergies were only a parsimonious description of the regularities in the muscle patterns generated by a nonmodular controller, we would expect adaptation rates to be similar, as both types of surgeries could be compensated with similar changes in the muscle patterns. In contrast, as predicted by modularity, we found strikingly faster adaptation after compatible surgeries than after incompatible ones. These results indicate that muscle synergies are key elements of a modular architecture underlying motor control and adaptation.

Effort minimization and synergistic muscle recruitment for three-dimensional force generation.

To generate a force at the hand in a given spatial direction and with a given magnitude the central nervous system (CNS) has to coordinate the recruitment of many muscles. Because of the redundancy in the musculoskeletal system, the CNS can choose one of infinitely many possible muscle activation patterns which generate the same force. What strategies and constraints underlie such selection is an open issue. The CNS might optimize a performance criterion, such as accuracy or effort. Moreover, the CNS might simplify the solution by constraining it to be a combination of a few muscle synergies, coordinated recruitment of groups of muscles. We tested whether the CNS generates forces by minimum effort recruitment of either individual muscles or muscle synergies. We compared the activation of arm muscles observed during the generation of isometric forces at the hand across multiple three-dimensional force targets with the activation predicted by either minimizing the sum of squared muscle activations or the sum of squared synergy activations. Muscle synergies were identified from the recorded muscle pattern using non-negative matrix factorization. To perform both optimizations we assumed a linear relationship between rectified and filtered electromyographic (EMG) signal which we estimated using multiple linear regressions. We found that the minimum effort recruitment of synergies predicted the observed muscle patterns better than the minimum effort recruitment of individual muscles. However, both predictions had errors much larger than the reconstruction error obtained by the synergies, suggesting that the CNS generates three-dimensional forces by sub-optimal recruitment of muscle synergies.