Can altered muscle synergies control unimpaired gait?

Recent studies have postulated that the human motor control system recruits groups of muscles through low-dimensional motor commands, or muscle synergies. This scheme simplifies the neural control problem associated with the high-dimensional structure of the neuromuscular system. Several lines of evidence have suggested that neurological injuries, such as stroke or cerebral palsy, may reduce the dimensions that are available to the motor control system, and these altered dimensions or synergies are thought to contribute to impaired walking patterns. However, no study has investigated whether impaired low-dimensional control spaces necessarily lead to impaired walking patterns. In this study, using a two-dimensional model of walking, we developed a synergy-based control framework that can simulate the dynamics of walking. The simulation analysis showed that a synergy-based control scheme can produce well-coordinated movements of walking matching unimpaired gait. However, when the dimensions available to the controller were reduced, the simplified emergent pattern deviated from unimpaired gait. A system with two synergies, similar to those seen after neurological injury, could not produce an unimpaired walking pattern. These findings provide further evidence that altered muscle synergies can contribute to impaired gait patterns and may need to be directly addressed to improve gait after neurological injury.     

Representation of movements and muscles within the primate precentral motor cortex: historical and current perspectives

A major problem with the study of the control of movement and posture is to determine how specific brain areas contribute to the selection of those particular muscle patterns that underlie a coordinated movement. With this problem in mind, a selective review is presented of mapping studies of the primate motor cortex, whose results bear on the question of how the spatial organization of cortical efferent cells might contribute to the production of organized muscle synergies. More recent findings are also summarized, which appear to resolve previous controversies on the question of whether movements or muscles are the primary units of motor cortex organization. These same findings suggest also a form of spatial organization within the primate precentral gyrus that would allow spatially simple afferent inputs to evoke the muscle synergies that are necessary for a variety of simple movements of the arm and hand.     

Muscle Synergies Heavily Influence the Neural Control of Arm Endpoint Stiffness and Energy Consumption

Much debate has arisen from research on muscle synergies with respect to both limb impedance control and energy consumption. Studies of limb impedance control in the context of reaching movements and postural tasks have produced divergent findings, and this study explores whether the use of synergies by the central nervous system (CNS) can resolve these findings and also provide insights on mechanisms of energy consumption. In this study, we phrase these debates at the conceptual level of interactions between neural degrees of freedom and tasks constraints. This allows us to examine the ability of experimentally-observed synergies—correlated muscle activations—to control both energy consumption and the stiffness component of limb endpoint impedance. In our nominal 6-muscle planar arm model, muscle synergies and the desired size, shape, and orientation of endpoint stiffness ellipses, are expressed as linear constraints that define the set of feasible muscle activation patterns. Quadratic programming allows us to predict whether and how energy consumption can be minimized throughout the workspace of the limb given those linear constraints. We show that the presence of synergies drastically decreases the ability of the CNS to vary the properties of the endpoint stiffness and can even preclude the ability to minimize energy. Furthermore, the capacity to minimize energy consumption—when available—can be greatly affected by arm posture. Our computational approach helps reconcile divergent findings and conclusions about task-specific regulation of endpoint stiffness and energy consumption in the context of synergies. But more generally, these results provide further evidence that the benefits and disadvantages of muscle synergies go hand-in-hand with the structure of feasible muscle activation patterns afforded by the mechanics of the limb and task constraints. These insights will help design experiments to elucidate the interplay between synergies and the mechanisms of learning, plasticity, versatility and pathology in neuromuscular systems.     

Strategy and synergy: two levels of equilibrium control during movement. Effects of the microgravity]

Equilibrium is ensured during forward or backward upper trunk movements by displacing the hip and knee simultaneously in opposite directions. When fast movements are performed, a muscle synergy characterized by the early activation of a set of trunk, thigh and leg muscles precedes the onset of the kinematic changes. The question which is addressed concerns the possibility that two levels of equilibrium control might exist during upper trunk movements: the strategy level, which is relatively invariant, is characterized by the displacement in opposite directions of the upper and low segments, and the muscle synergy level at which the strategy is implemented, which may be adaptable to the environmental constraints. When upper trunk movements are performed under microgravity with the subject's feet fixed to the floor of the space cabin, the displacement of upper and lower body segments in opposite directions still occurs, although this is no longer necessary to maintain the equilibrium. This kinematic strategy seems to be aimed at regulating the centre of inertia position with respect to the feet. The muscle synergies associated with these kinematic changes are modified, however, under microgravity. After returning to the ground, the previous synergies do not reappear immediately, but only after a few days. This suggests that a short period of learning is needed to change the synergy. These data are compatible with the hypothesis that two levels of equilibrium control actually exist during upper trunk movements, the strategy level, which is kinematic and invariant, and the synergy level, which is adaptable to the environmental constraints through a short learning process.     

Functional muscle synergies to support the knee against moment specific loads while weight bearing

ObjectiveExternally applied abduction and rotational loads are major contributors to the knee joint injury mechanism; yet, how muscles work together to stabilize the knee against these loads remains unclear. Our study sought to evaluate lower limb functional muscle synergies in healthy young adults such that muscle activation can be directly related to internal knee joint moments.MethodsConcatenated non-negative matrix factorization extracted muscle and moment synergies of 22 participants from electromyographic signals and joint moments elicited during a weight-bearing force matching protocol.ResultsTwo synergy sets were extracted: Set 1 included four synergies, each corresponding to a general anterior, posterior, medial, or lateral force direction. Frontal and transverse moments were coupled during medial and lateral force directions. Set 2 included six synergies, each corresponding to a moment type (extension/flexion, ab/adduction, internal/external rotation). Hamstrings and quadriceps dominated synergies associated with respective flexion and extension moments while quadriceps-hamstring co-activation was associated with knee abduction. Rotation moments were associated with notable contributions from hamstrings, quadriceps, gastrocnemius, and hip ab/adductors, corresponding to a general co-activation muscle synergy.ConclusionOur results highlight the importance of muscular co-activation of all muscles crossing the knee to support it during injury-inducing loading conditions such as externally applied knee abduction and rotation. Functional muscle synergies can provide new insight into the relationship between neuromuscular control and knee joint stability by directly associating biomechanical variables to muscle activation.     

Optimization of muscle activity for task-level goals predicts complex changes in limb forces across biomechanical contexts

Optimality principles have been proposed as a general framework for understanding motor control in animals and humans largely based on their ability to predict general features movement in idealized motor tasks. However, generalizing these concepts past proof-of-principle to understand the neuromechanical transformation from task-level control to detailed execution-level muscle activity and forces during behaviorally-relevant motor tasks has proved difficult. In an unrestrained balance task in cats, we demonstrate that achieving task-level constraints center of mass forces and moments while minimizing control effort predicts detailed patterns of muscle activity and ground reaction forces in an anatomically-realistic musculoskeletal model. Whereas optimization is typically used to resolve redundancy at a single level of the motor hierarchy, we simultaneously resolved redundancy across both muscles and limbs and directly compared predictions to experimental measures across multiple perturbation directions that elicit different intra- and interlimb coordination patterns. Further, although some candidate task-level variables and cost functions generated indistinguishable predictions in a single biomechanical context, we identified a common optimization framework that could predict up to 48 experimental conditions per animal (n = 3) across both perturbation directions and different biomechanical contexts created by altering animals' postural configuration. Predictions were further improved by imposing experimentally-derived muscle synergy constraints, suggesting additional task variables or costs that may be relevant to the neural control of balance. These results suggested that reduced-dimension neural control mechanisms such as muscle synergies can achieve similar kinetics to the optimal solution, but with increased control effort (≈2×) compared to individual muscle control. Our results are consistent with the idea that hierarchical, task-level neural control mechanisms previously associated with voluntary tasks may also be used in automatic brainstem-mediated pathways for balance.     

Neuromechanics of muscle synergies for posture and movement

Recent research suggests that the nervous system controls muscles by activating flexible combinations of muscle synergies to produce a wide repertoire of movements. Muscle synergies are like building blocks, defining characteristic patterns of activation across multiple muscles that may be unique to each individual, but perform similar functions. The identification of muscle synergies has strong implications for the organization and structure of the nervous system, providing a mechanism by which task-level motor intentions are translated into detailed, low-level muscle activation patterns. Understanding the complex interplay between neural circuits and biomechanics that give rise to muscle synergies will be crucial to advancing our understanding of neural control mechanisms for movement.     

Muscle synergies underlying sit-to-stand tasks in elderly people and their relationship with kinetic characteristics

BackgroundPhysiological evidence suggests that the nervous system controls motion by using a low-dimensional synergy organization for muscle activation. Because the muscle activation produces joint torques, kinetic changes accompanying aging can be related to changes in muscle synergies.ObjectivesWe explored the effects of aging on muscle synergies underlying sit-to-stand tasks, and examined their relationships with kinetic characteristics.MethodsFour younger and three older adults performed the sit-to-stand task at two speeds. Subsequently, we extracted the muscle synergies used to perform these tasks. Hierarchical cluster analysis was used to classify these synergies. We also calculated kinetic variables to compare the groups.ResultsThree independent muscle synergies generally appeared in each subject. The spatial structure of these synergies was similar across age groups. The change in motion speed affected only the temporal structure of these synergies. However, subject-specific muscle synergies and kinetic variables existed.ConclusionsOur results suggest common muscle synergies underlying the sit-to-stand task in both young and elderly adults. People may actively change only the temporal structure of each muscle synergy. The precise subject-specific structuring of each muscle synergy may incorporate knowledge of the musculoskeletal kinetics.     

Myosin filament structure in vertebrate smooth muscle

The in vivo structure of the myosin filaments in vertebrate smooth muscle is unknown. Evidence from purified smooth muscle myosin and from some studies of intact smooth muscle suggests that they may have a nonhelical, side-polar arrangement of crossbridges. However, the bipolar, helical structure characteristic of myosin filaments in striated muscle has not been disproved for smooth muscle. We have used EM to investigate this question in a functionally diverse group of smooth muscles (from the vascular, gastrointestinal, reproductive, and visual systems) from mammalian, amphibian, and avian species. Intact muscle under physiological conditions, rapidly frozen and then freeze substituted, shows many myosin filaments with a square backbone in transverse profile. Transverse sections of fixed, chemically skinned muscles also show square backbones and, in addition, reveal projections (crossbridges) on only two opposite sides of the square. Filaments gently isolated from skinned smooth muscles and observed by negative staining show crossbridges with a 14.5-nm repeat projecting in opposite directions on opposite sides of the filament. Such filaments subjected to low ionic strength conditions show bare filament ends and an antiparallel arrangement of myosin tails along the length of the filament. All of these observations are consistent with a side-polar structure and argue against a bipolar, helical crossbridge arrangement. We conclude that myosin filaments in all smooth muscles, regardless of function, are likely to be side-polar. Such a structure could be an important factor in the ability of smooth muscles to contract by large amounts.     

The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ

Background

Like human infants, songbirds learn their species-specific vocalizations through imitation learning. The birdsong system has emerged as a widely used experimental animal model for understanding the underlying neural mechanisms responsible for vocal production learning. However, how neural impulses are translated into the precise motor behavior of the complex vocal organ (syrinx) to create song is poorly understood. First and foremost, we lack a detailed understanding of syringeal morphology.

Results

To fill this gap we combined non-invasive (high-field magnetic resonance imaging and micro-computed tomography) and invasive techniques (histology and micro-dissection) to construct the annotated high-resolution three-dimensional dataset, or morphome, of the zebra finch (Taeniopygia guttata) syrinx. We identified and annotated syringeal cartilage, bone and musculature in situ in unprecedented detail. We provide interactive three-dimensional models that greatly improve the communication of complex morphological data and our understanding of syringeal function in general.

Conclusions

Our results show that the syringeal skeleton is optimized for low weight driven by physiological constraints on song production. The present refinement of muscle organization and identity elucidates how apposed muscles actuate different syringeal elements. Our dataset allows for more precise predictions about muscle co-activation and synergies and has important implications for muscle activity and stimulation experiments. We also demonstrate how the syrinx can be stabilized during song to reduce mechanical noise and, as such, enhance repetitive execution of stereotypic motor patterns. In addition, we identify a cartilaginous structure suited to play a crucial role in the uncoupling of sound frequency and amplitude control, which permits a novel explanation of the evolutionary success of songbirds.     

Synergistic co-activation in multi-directional postural control in humans

To examine the muscle synergies of multi-directional postural control, we calculated the target-directed variance fraction (η) and net action direction of each muscle using the electromyogram-weighted averaging (EWA) method. Subjects stood barefoot on a force platform and maintained their posture by producing a center of pressure (COP) in twelve target directions. Surface electromyograms were recorded from 6 right-sided muscles: tibialis anterior (TA), soleus (SOL), lateral gastrocnemius (LG), medial gastrocnemius (MG), fibularis longus (FL), and gluteus medius (GM). η was calculated from COP with duration of 20-s, during which the COP was relatively constant. The EWA method was applied to the EMG and the two COP components to estimate the net action direction of each muscle. The results showed that η values in all directions did not cross the 0.8 threshold. This suggests that human postural control is achieved by synergistic co-activation. The EWA revealed that the net action directions of TA, SOL, LG, MG, and GM were 277.6°, 71.1°, 87.7°, 94.0°, and 2.2°, respectively. This suggests that postural maintenance by muscle synergy can be attributed to the relevant muscles having various action directions. These results demonstrate that muscle synergies can be investigated using COP fluctuations.     

The integration of lateral gastrocnemius muscle function and kinematics in running turkeys

Animals commonly move over a range of speeds, and encounter considerable variation in habitat structure, such as inclines. Hindlimb kinematics and muscle function in diverse groups of vertebrates are affected by these changes in behavior and habitat structure, providing a fruitful source of variation for studying the integration of kinematics and muscle function. While it has been observed in a variety of vertebrates that muscle length change can be minimal during locomotion, it is unclear how, and to what degree, in vivo muscle length change patterns are integrated with kinematics. We tested the hypothesis that the length of the turkey lateral gastrocnemius (LG), a biarticular muscle that has moments at the ankle and knee, is not solely affected by changes in joint kinematics. We recorded in vivo muscle length changes (using sonomicrometry) and hindlimb movements (using high-speed video) of wild turkeys running on various inclines, and at different speeds. We quantified the relationship between joint angle (knee and ankle separately) and muscle length in freshly euthanized specimens, and then applied an empirically derived correction for changes in pennation angle and tendon strain during locomotion to improve the accuracy of our predicted lengths. We estimated muscle length at four points during each stride and then compared these values with those measured directly. Other than during swing, the predicted changes in muscle length calculated from the changes in joint kinematics did not correspond with our measured values of LG length. Therefore, the lengths at which the LG operates in turkeys are not determined entirely by kinematics. In addition to strain in series elastic components, we hypothesize that heterogeneous strain within muscles, interactions between muscles and muscle pennation angle all contribute to the nonlinear relationship between muscle length changes and kinematics.     

Functional muscle synergies constrain force production during postural tasks

We recently demonstrated that a set of five functional muscle synergies were sufficient to characterize both hindlimb muscle activity and active forces during automatic postural responses in cats standing at multiple postural configurations. This characterization depended critically upon the assumption that the endpoint force vector (synergy force vector) produced by the activation of each muscle synergy rotated with the limb axis as the hindlimb posture varied in the sagittal plane. Here, we used a detailed, 3D static model of the hindlimb to confirm that this assumption is biomechanically plausible: as we varied the model posture, simulated synergy force vectors rotated monotonically with the limb axis in the parasagittal plane (r2=0.94+/-0.08). We then tested whether a neural strategy of using these five functional muscle synergies provides the same force-generating capability as controlling each of the 31 muscles individually. We compared feasible force sets (FFSs) from the model with and without a muscle synergy organization. FFS volumes were significantly reduced with the muscle synergy organization (F=1556.01, p<0.01), and as posture varied, the synergy-limited FFSs changed in shape, consistent with changes in experimentally measured active forces. In contrast, nominal FFS shapes were invariant with posture, reinforcing prior findings that postural forces cannot be predicted by hindlimb biomechanics alone. We propose that an internal model for postural force generation may coordinate functional muscle synergies that are invariant in intrinsic limb coordinates, and this reduced-dimension control scheme reduces the set of forces available for postural control.     

Influence of locomotion speed on biomechanical subtask and muscle synergy

This paper investigates the relationship of biomechanical subtasks, and muscle synergies with various locomotion speeds. Ground reaction force (GRF) of eight healthy subjects is measured synchronously by force plates of treadmill at five different speeds ranging from 0.5 m/s to 1.5 m/s. Four basic biomechanical subtasks, body support, propulsion, swing, and heel strike preparation, are identified according to GRF. Meanwhile, electromyography (EMG) data, used to extract muscle synergies, are collected from lower limb muscles. EMG signals are segmented periodically based on GRF with the heel strike as the split points. Variability accounted for (VAF) is applied to determine the number of muscle synergies. We find that four muscle synergies can be extracted in all five situations by non-negative matrix factorization (NMF). Furthermore, the four muscle synergies and biomechanical subtasks keep invariant as the walking speed changes.     

Inter-joint coupling effects on muscle contributions to endpoint force and acceleration in a musculoskeletal model of the cat hindlimb

The biomechanical principles underlying the organization of muscle activation patterns during standing balance are poorly understood. The goal of this study was to understand the influence of biomechanical inter-joint coupling on endpoint forces and accelerations induced by the activation of individual muscles during postural tasks. We calculated induced endpoint forces and accelerations of 31 muscles in a 7 degree-of-freedom, three-dimensional model of the cat hindlimb. To test the effects of inter-joint coupling, we systematically immobilized the joints (excluded kinematic degrees of freedom) and evaluated how the endpoint force and acceleration directions changed for each muscle in 7 different conditions. We hypothesized that altered inter-joint coupling due to joint immobilization of remote joints would substantially change the induced directions of endpoint force and acceleration of individual muscles. Our results show that for most muscles crossing the knee or the hip, joint immobilization altered the endpoint force or acceleration direction by more than 90° in the dorsal and sagittal planes. Induced endpoint forces were typically consistent with behaviorally observed forces only when the ankle was immobilized. We then activated a proximal muscle simultaneous with an ankle torque of varying magnitude, which demonstrated that the resulting endpoint force or acceleration direction is modulated by the magnitude of the ankle torque. We argue that this simple manipulation can lend insight into the functional effects of co-activating muscles. We conclude that inter-joint coupling may be an essential biomechanical principle underlying the coordination of proximal and distal muscles to produce functional endpoint actions during motor tasks.     

A model for insect locomotion in the horizontal plane: Feedforward activation of fast muscles, stability, and robustness

We develop a neuromechanical model for running insects that includes a simplified hexapedal leg geometry with agonist-antagonist muscle pairs actuating each leg joint. Restricting to dynamics in the horizontal plane and neglecting leg masses, we reduce the model to three degrees of freedom describing translational and yawing motions of the body. Muscles are driven by stylized action potentials characteristic of fast motoneurons, and modeled using an activation function and nonlinear length and shortening velocity dependence. Parameter values are based on measurements from depressor muscles and observations of kinematics and dynamics of the cockroach Blaberus discoidalis; in particular, motoneuronal inputs and muscle force levels are chosen to approximately achieve joint torques that are consistent with measured ground reaction forces. We show that the model has stable double-tripod gaits over the animal's speed range, that its dynamics at preferred speeds matches those observed, and that it maintains stable gaits, with low frequency yaw deviations, when subject to random perturbations in foot touchdown and lift-off timing and action potential input timing. We explain this in terms of the low-dimensional dynamics.     

Dual Dimensionality Reduction Reveals Independent Encoding of Motor Features in a Muscle Synergy for Insect Flight Control

What are the features of movement encoded by changing motor commands? Do motor commands encode movement independently or can they be represented in a reduced set of signals (i.e. synergies)? Motor encoding poses a computational and practical challenge because many muscles typically drive movement, and simultaneous electrophysiology recordings of all motor commands are typically not available. Moreover, during a single locomotor period (a stride or wingstroke) the variation in movement may have high dimensionality, even if only a few discrete signals activate the muscles. Here, we apply the method of partial least squares (PLS) to extract the encoded features of movement based on the cross-covariance of motor signals and movement. PLS simultaneously decomposes both datasets and identifies only the variation in movement that relates to the specific muscles of interest. We use this approach to explore how the main downstroke flight muscles of an insect, the hawkmoth Manduca sexta, encode torque during yaw turns. We simultaneously record muscle activity and turning torque in tethered flying moths experiencing wide-field visual stimuli. We ask whether this pair of muscles acts as a muscle synergy (a single linear combination of activity) consistent with their hypothesized function of producing a left-right power differential. Alternatively, each muscle might individually encode variation in movement. We show that PLS feature analysis produces an efficient reduction of dimensionality in torque variation within a wingstroke. At first, the two muscles appear to behave as a synergy when we consider only their wingstroke-averaged torque. However, when we consider the PLS features, the muscles reveal independent encoding of torque. Using these features we can predictably reconstruct the variation in torque corresponding to changes in muscle activation. PLS-based feature analysis provides a general two-sided dimensionality reduction that reveals encoding in high dimensional sensory or motor transformations.     

A model for neural control of gradation of muscle force

A mathematical muscle model is presented that relates neural control signals linearly to muscle force without violating important known physiological constraints, such as the size-principle (Henneman and Mendell 1981) and non-linear twitch summation (Burke et al. 1976). This linearity implies that the neural control signals (defined as a weighted sum of activities in a nerve bundle) can be interpreted as the internal representation of total muscle force. The model allows for different relative contributions from the two force-grading mechanisms, i.e. the recruitment of motor units and the modulation of their firing frequency. It can therefore be applied to a variety of (distal and proximal) muscles. Furthermore, it permits simple mechanisms for controlling muscle force, e.g. in superposed motor tasks. The model confirms our intuitive notion that a weighted sum of activities in a nerve bundle can directly represent an external controlled variable, which in this case is exerted muscle force.     

Muscle recruitment and coordination with an ankle exoskeleton

Exoskeletons have the potential to assist and augment human performance. Understanding how users adapt their movement and neuromuscular control in response to external assistance is important to inform the design of these devices. The aim of this research was to evaluate changes in muscle recruitment and coordination for ten unimpaired individuals walking with an ankle exoskeleton. We evaluated changes in the activity of individual muscles, cocontraction levels, and synergistic patterns of muscle coordination with increasing exoskeleton work and torque. Participants were able to selectively reduce activity of the ankle plantarflexors with increasing exoskeleton assistance. Increasing exoskeleton net work resulted in greater reductions in muscle activity than increasing exoskeleton torque. Patterns of muscle coordination were not restricted or constrained to synergistic patterns observed during unassisted walking. While three synergies could describe nearly 95% of the variance in electromyography data during unassisted walking, these same synergies could describe only 85–90% of the variance in muscle activity while walking with the exoskeleton. Synergies calculated with the exoskeleton demonstrated greater changes in synergy weights with increasing exoskeleton work versus greater changes in synergy activations with increasing exoskeleton torque. These results support the theory that unimpaired individuals do not exclusively use central pattern generators or other low-level building blocks to coordinate muscle activity, especially when learning a new task or adapting to external assistance, and demonstrate the potential for using exoskeletons to modulate muscle recruitment and coordination patterns for rehabilitation or performance.     

Three-dimensional model to predict muscle forces and their relation to motor variances in reaching arm movements

A three-dimensional (3-D) arm movement model is presented to simulate kinematic properties and muscle forces in reaching arm movements. Healthy subjects performed reaching movements repetitively either with or without a load in the hand. Joint coordinates were measured. Muscle moment arms, 3-D angular acceleration, and moment of inertias of arm segments were calculated to determine 3-D joint torques. Variances of hand position, arm configuration, and muscle activities were calculated. Ratios of movement variances observed in the two conditions (load versus without load) showed no differences for hand position and arm configuration variances. Virtual muscle force variances for all muscles except deltoid posterior and EMG variances for four muscles increased significantly by moving with the load. The greatly increased variances in muscle activity did not imply equally high increments in kinematic variances. We conclude that enhanced muscle cooperation through synergies helps to stabilize movement at the kinematic level when a load is added.