Andrea d'Avella

Combinations of muscle synergies in the construction of a natural motor behavior

A central issue in motor control is how the central nervous system generates the muscle activity patterns necessary to achieve a variety of behavioral goals. The many degrees of freedom of the musculoskeletal apparatus provide great flexibility but make the control problem extremely complex. Muscle synergies—coherent activations, in space or time, of a group of muscles—have been proposed as building blocks that could simplify the construction of motor behaviors. To evaluate this hypothesis, we developed a new method to extract invariant spatiotemporal components from the simultaneous recordings of the activity of many muscles. We used this technique to analyze the muscle patterns of intact and unrestrained frogs during kicking, a natural defensive behavior. Here we show that combinations of three time-varying muscle synergies underlie the variety of muscle patterns required to kick in different directions, that the recruitment of these synergies is related to movement kinematics, and that there are similarities among the synergies extracted from different behaviors.

Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors

Previous studies have suggested that the motor system may simplify control by combining a small number of muscle synergies represented as activation profiles across a set of muscles. The role of sensory feedback in the activation and organization of synergies has remained an open question. Here, we assess to what extent the motor system relies on centrally organized synergies activated by spinal and/or supraspinal commands to generate motor outputs by analyzing electromyographic (EMG) signals collected from 13 hindlimb muscles of the bullfrog during swimming and jumping, before and after deafferentation. We first established that, for both behaviors, the intact and deafferented data sets possess low and similar dimensionalities. Subsequently, we used a novel reformulation of the non-negative matrix factorization algorithm to simultaneously search for synergies shared by, and synergies specific to, the intact and deafferented data sets. Most muscle synergies were identified as shared synergies, suggesting that EMGs of locomotor behaviors are generated primarily by centrally organized synergies. Both the amplitude and temporal patterns of the activation coefficients of most shared synergies, however, were altered by deafferentation, suggesting that sensory inflow modulates activation of those centrally organized synergies. For most synergies, effects of deafferentation on the activation coefficients were not consistent across frogs, indicating substantial interanimal variability of feedback actions. We speculate that sensory feedback might adapt recruitment of muscle synergies to behavioral constraints, and the few synergies specific to the intact or deafferented states might represent afferent-specific modules or feedback reorganization of spinal neuronal networks.

Modulation of phasic and tonic muscle synergies with reaching direction and speed

How the CNS masters the many degrees of freedom of the musculoskeletal system to control goal-directed movements is a long-standing question. We have recently provided support to the hypothesis that the CNS relies on a modular control architecture by showing that the phasic muscle patterns for fast reaching movements in different directions are generated by combinations of a few time-varying muscle synergies: coordinated recruitment of groups of muscles with specific activation profiles. However, natural reaching movements occur at different speeds and require the control of both movement and posture. Thus we have investigated whether muscle synergies also underlie reaching at different speeds as well as the maintenance of stable arm postures. Hand kinematics and shoulder and elbow muscle surface EMGs were recorded in five subjects during reaches to eight targets in the frontal plane at different speeds. We found that the amplitude modulation of three time-invariant synergies captured the variations in the postural muscle patterns at the end of the movement. During movement, three phasic and three tonic time-varying synergies could reconstruct the time-normalized muscle pattern in all conditions. Phasic synergies were modulated in both amplitude and timing by direction and speed. Tonic synergies were modulated only in amplitude by direction. The directional tuning of both types of synergies was well described by a single or a double cosine function. These results suggest that muscle synergies are basic control modules that allow generating the appropriate muscle patterns through simple modulation and combination rules.

Modulation of muscle synergy recruitment in primate grasping.

In grasping, the CNS controls a particularly large number of degrees of freedom. We tested the idea that this control is facilitated by the presence of muscle synergies. According to the strong version of this concept, these synergies are invariant, hard-wired patterns of activation across muscles. Synergies may serve as modules that linearly sum, each with specific amplitude and timing coefficients, to generate a large array of muscle patterns. We tested two predictions of the synergy model. A small number of synergies should (1) account for a large fraction of variation in muscle activity, and (2) be modulated in their recruitment by task variables, even in novel behavioral contexts. We also examined whether the synergies would (3) have broadly similar structures across animals. We recorded from 15 to 19 electrodes implanted in forelimb muscles of two rhesus macaques as they grasped and transported 25 objects of variable shape and size. We show that three synergies accounted for 81% of the electromyographic data variation in each monkey. Each synergy was modulated in its recruitment strength and/or timing by object shape and/or size. Even when synergies were extracted from a small subset of object shape and size conditions and then used to reconstruct the entire dataset, we observed highly similar synergies and patterns of modulation. The synergies were well conserved between monkeys, with two of the synergies exceeding chance structural similarity, and the third being recruited, in both animals, in proportion to the size of the object handled.

Coordination and localization in spinal motor systems.

We review here experiments examining the hypothesis that vertebrate spinal motor systems produce movement through the flexible combination of a small number of units of motor output. Using a variety of preparations and techniques, these experiments provide evidence for such spinally generated units and for the localization of the networks responsible for producing them within different regions of the spinal cord. Such an organization might help to simplify the production of movement, reducing the degrees of freedom that need to be specified by providing a set of units involved in regulating features common to a range of behaviors.

Identifying representative synergy matrices for describing muscular activation patterns during multidirectional reaching in the horizontal plane.

Muscle synergies have been proposed as a simplifying principle of generation of movements based on a low-dimensional control by the CNS. This principle may be useful for movement restoration by, e.g., functional electrical stimulation (FES), if a limited set of synergies can describe several functional tasks. This study investigates the possibility of describing a multijoint reaching task of the upper limb by a linear combination of one set of muscle synergies common to multiple directions. Surface electromyographic (EMG) signals were recorded from 12 muscles of the dominant upper limb of eight healthy men during single-joint movements and a multijoint reaching task in 12 directions in the horizontal plane. The movement kinematics was recorded by a motion analysis system. Muscle synergies were extracted with nonnegative matrix factorization of the EMG envelopes. Synergies were computed either from the single-joint movements to describe the two degrees of freedom independently or from the multijoint movements. On average, the multijoint reaching task could be accurately described in all the directions (coefficient of determination >0.85) by a linear combination of either four synergies extracted from the individual degrees of freedom or three synergies extracted from multijoint movements in at least three reaching directions. These results indicate that a large set of multijoint movements can be generated by a synergy matrix of limited dimensionality and common to all directions if the synergies are extracted from a representative number of directions. The linear combination of synergies may thus be used in strategies for restoring functions, such as FES.

Modular organization of spinal motor systems.

The vertebrate nervous system produces a wide range of movement flexibly and efficiently, even though the simplest of these movements is potentially highly complex. The strategies by which the nervous system overcomes these complexities have therefore been of interest to motor physiologists for decades. In this review, the authors present a number of recent experiments that propose one strategy by which the nervous system might simplify the production of movement. These experiments suggest that spinal motor systems are organized in terms of a small number of distinct motor responses, or “modules.” These distinct modules can be combined together simply to produce a wide range of different movements. Such a modular organization of spinal motor systems can potentially allow the nervous system to produce a wide range of natural behaviors in a simple and flexible manner.

On the Origin of Planar Covariation of Elevation Angles During Human Locomotion

Leg segment rotations in human walking covary, so that the three-dimensional trajectory of temporal changes in the elevation angles lies close to a plane. Recently the role of central versus biomechanical constraints on the kinematics control of human locomotion has been questioned. Here we show, based on both modeling and experimental data, that the planar law of intersegmental coordination is not a simple consequence of biomechanics. First, the full limb behavior in various locomotion modes (walking on inclined surface, staircase stepping, air-stepping, crouched walking, hopping) can be expressed as 2 degrees of freedom planar motion even though the orientation of the plane and pairwise segment angle correlations may differ substantially. Second, planar covariation is not an inevitable outcome of any locomotor movement. It can be systematically violated in some conditions (e.g., when stooping and grasping an object on the floor during walking or in toddlers at the onset of independent walking) or transferred into a simple linear relationship in others (e.g., during stepping in place). Finally, all three major limb segments contribute importantly to planar covariation and its characteristics resulting in a certain endpoint trajectory defined by the limb axis length and orientation. Recent advances in the neural control of movement support the hypothesis about central representation of kinematics components.

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.

Adjustments of Motor Pattern for Load Compensation Via Modulated Activations of Muscle Synergies During Natural Behaviors

It has been suggested that the motor system may circumvent the difficulty of controlling many degrees of freedom in the musculoskeletal apparatus by generating motor outputs through a combination of discrete muscle synergies. How a discretely organized motor system compensates for diverse perturbations has remained elusive. Here, we investigate whether motor responses observed after an inertial-load perturbation can be generated by altering the recruitment of synergies normally used for constructing unperturbed movements. Electromyographic (EMG, 13 muscles) data were collected from the bullfrog hindlimb during natural behaviors before, during, and after the same limb was loaded by a weight attached to the calf. Kinematic analysis reveals the absence of aftereffect on load removal, suggesting that load-related EMG changes were results of immediate motor pattern adjustments. We then extracted synergies from EMGs using the nonnegative matrix factorization algorithm and developed a procedure for assessing the extent of synergy sharing across different loading conditions. Most synergies extracted were found to be activated in all loaded and unloaded conditions. However, for certain synergies, the amplitude, duration, and/or onset time of their activation bursts were up- or down-modulated during loading. Behavioral parameterizations reveal that load-related modulation of synergy activations depended on the behavioral variety (e.g., kick direction and amplitude) and the movement phase performed. Our results suggest that muscle synergies are robust across different dynamic conditions and immediate motor adjustments can be accomplished by modulating synergy activations. An appendix describes the novel procedure we developed, useful for discovering shared and specific features from multiple data sets.