Muscle synergy

EC Kuska, KM Steele (2024) “Does crouch alter the effects of neuromuscular impairments on gait? A simulation study”

Katie Landwehr JournalArticle, MotorControl, Publications , , , , , ,

Journal Article in Journal of Biomechanics

Cerebral palsy (CP) is a neurologic injury that impacts control of movement. Individuals with CP also often develop secondary impairments like weakness and contracture. Both altered motor control and secondary impairments influence how an individual walks after neurologic injury. However, understanding the complex interactions between and relative effects of these impairments makes analyzing and improving walking capacity in CP challenging.

A sagittal-plane musculoskeletal model and neuromuscular simulation framework that tracked average nondisabled (ND) kinematics and moderate and severe crouch gait. The model contains nine degrees-of-freedom (pelvic tilt and translation, and right and left hip, knee, and ankle flexion) actuated by eight Hill-type musculotendinous units per leg. The objective function minimized deviations from tracked kinematics and the sum of muscle activations squared (a2). We perturbed each gait simulation with multi-modal neuromuscular impairments—altered control, weakness, and contracture—of varying severities. Altered control was simulated by reducing the number of fixed synergies controlling each leg, and weakness and contracture were simulated by reducing a muscle’s maximum isometric force ( ) and tendon slack length ( ), respectively. A Bayesian Additive Regression Trees (BART) model then predicted resultant a2 from the simulated neuromuscular impairments for crouch and ND gait to evaluate the relative effects of each simulated neuromuscular impairment on the muscle activations required to maintain each gait pattern.Aim: The purpose of this study was to investigate the interactions between neuromuscular impairments and gait in CP.

Methods: We used a sagittal-plane musculoskeletal model and neuromuscular control framework to simulate crouch and nondisabled gait. We perturbed each simulation by varying the number of synergies controlling each leg (altered control), and imposed weakness and contracture. A Bayesian Additive Regression Trees (BART) model was also used to parse the relative effects of each impairment on the muscle activations required for each gait pattern.

Results: By using these simulations to evaluate gait-pattern specific effects of neuromuscular impairments, we identified some advantages of crouch gait. For example, crouch tolerated 13 % and 22 % more plantarflexor weakness than nondisabled gait without and with altered control, respectively. Furthermore, BART demonstrated that plantarflexor weakness had twice the effect on total muscle activity required during nondisabled gait than crouch gait. However, crouch gait was also disadvantageous in the presence of vasti weakness: crouch gait increased the effects of vasti weakness on gait without and with altered control.

Interpretation: These simulations highlight gait-pattern specific effects and interactions between neuromuscular impairments. Utilizing computational techniques to understand these effects can elicit advantages of gait deviations, providing insight into why individuals may select their gait pattern and possible interventions to improve energetics.

AM Spomer, RZ Yan, MH Schwartz, KM Steele (2023) “Motor control complexity can be dynamically simplified during gait pattern exploration using motor control-based biofeedback”

Katie Landwehr JournalArticle, MotorControl, News, Projects, Publications , , , , , ,

Journal Article in Journal of Neurophysiology

Understanding how the central nervous system coordinates diverse motor outputs has been a topic of extensive investigation. Although it is generally accepted that a small set of synergies underlies many common activities, such as walking, whether synergies are equally robust across a broader array of gait patterns or can be flexibly modified remains unclear.

Schematic of the custom biofeedback system. A) Motor control biofeedback used to encourage pattern exploration. B) Individuals significantly modified motor control complexity using biofeedback. C) Distal gait mechanics were associated with changes in control complexity.Aim: The aim of this study was to characterize the robustness of synergies to changing biomechanical constraints during walking. Specifically, we evaluated the extent to which nondisabled individuals could modulate both synergy structure and complexity while using motor control biofeedback to drive broad gait pattern exploration.

Methods: We evaluated the extent to which synergies changed as nondisabled adults (n = 14) explored gait patterns using custom biofeedback. Secondarily, we used Bayesian additive regression trees to identify factors that were associated with synergy modulation.

Results: Participants explored 41.1 ± 8.0 gait patterns using biofeedback, during which synergy recruitment changed depending on the type and magnitude of gait pattern modification. Specifically, a consistent set of synergies was recruited to accommodate small deviations from baseline, but additional synergies emerged for larger gait changes. Synergy complexity was similarly modulated; complexity decreased for 82.6% of the attempted gait patterns, but distal gait mechanics were strongly associated with these changes. In particular, greater ankle dorsiflexion moments and knee flexion through stance, as well as greater knee extension moments at initial contact, corresponded to a reduction in synergy complexity.

Interpretation: Taken together, these results suggest that the central nervous system preferentially adopts a low-dimensional, largely invariant control strategy but can modify that strategy to produce diverse gait patterns. Beyond improving understanding of how synergies are recruited during gait, study outcomes may also help identify parameters that can be targeted with interventions to alter synergies and improve motor control after neurological injury.

New & Noteworthy: We used a motor control-based biofeedback system and machine learning to characterize the extent to which nondisabled adults can modulate synergies during gait pattern exploration. Results revealed that a small library of synergies underlies an array of gait patterns but that recruitment from this library changes as a function of the imposed biomechanical constraints. Our findings enhance understanding of the neural control of gait and may inform biofeedback strategies to improve synergy recruitment after neurological injury.

BC Conner, AM Spomer, SSPA Bishe, KM Steele, ZF Lerner (2022) “Soleus H-reflex modulation in cerebral palsy and its relationship with neural control complexity: a pilot study”

Katie Landwehr JournalArticle, MotorControl, News, Publications , , ,

Journal Article in Experimental Brain Research

Individuals with cerebral palsy (CP) display motor control patterns that suggest decreased supraspinal input, but it remains unknown if they are able to modulate lower-limb reflexes in response to more complex tasks, or whether global motor control patterns relate to reflex modulation capacity in this population.

Figure 1) Study design. (A) Task complexity protocol, where soleus H-reflexes were elicited with stimulation of the posterior tibial nerve under two conditions: a baseline, bilateral standing condition and a complex, unilateral standing condition (B) Walking ankle resistance protocol, where soleus H-reflexes were elicited during mid-stance under a baseline walking and when walking with an ankle exoskeleton device delivering resistance to plantar flexion proportional to a user’s real-time estimated ankle moment.Aim:  To further elucidate the multifaceted effects of CP on inhibitory and faciliatory supraspinal pathways and global measures of motor control, providing novel information for improving targeted neuromuscular interventions in this patient population.

Methods: Eight ambulatory individuals with CP (12–18 years old) were recruited to complete a task complexity protocol, where soleus H-reflex excitability was compared between bilateral (baseline) and unilateral (complex) standing. We also investigated the relationship between each participant’s ability to modulate soleus H-reflex excitability and the complexity of their walking neural control pattern determined from muscle synergy analysis. Finally, six of the eight participants completed an exoskeleton walking protocol, where soleus H-reflexes were collected during the stance phase of walking with and without stance-phase plantar flexor resistance.

Results: Participants displayed a significant reduction in soleus H-reflex excitability (− 26 ± 25%, p = 0.04) with unilateral standing, and a strong positive relationship was observed between more refined neural control during walking and an increased ability to modulate reflex excitability (R = 0.79, p = 0.04). There was no difference in neuromuscular outcome measures with and without the ankle exoskeleton (p values all > 0.05), with variable reflex responses to walking with ankle exoskeleton resistance.

Interpretation: These findings provide evidence that ambulatory individuals with CP retain some capacity to modulate lower-limb reflexes in response to increased task complexity, and that less refined neural control during walking appears to be related to deficits in reflex modulation.

EC Kuska, N Mehrabi, MH Schwartz, KM Steele (2022) “Number of synergies impacts sensitivity of gait to weakness and contracture”

Katie Landwehr JournalArticle, MotorControl, News, Projects, Publications , , , , , ,

Journal Article in Journal of Biomechanics

Muscle activity during gait can be described by a small set of synergies, weighted groups of muscles, that are theorized to reflect underlying neural control. For people with neurologic injuries, like cerebral palsy or stroke, even fewer synergies are required to explain muscle activity during gait. This reduction in synergies is thought to reflect altered control and is associated with impairment severity and treatment outcomes. Individuals with neurologic injuries also develop secondary musculoskeletal impairments, like weakness or contracture, that can impact gait. Yet, the combined impacts of altered control and musculoskeletal impairments on gait remains unclear.

A two-dimensional sagittal plane musculoskeletal model and synergy simulation framework tracked unimpaired gait kinematics. The model had nine degrees of freedom, including right and left leg hip, knee, and ankle flexion, actuated by eight muscles per leg. Fixed sets of synergies constrained control, forcing the direct collocation algorithm to solve for synergy activations. The objective function minimized deviations from unimpaired kinematics and the sum of muscle activations squared (neural demand). Weakness, simulated by a reduction in maximum isometric force, and contracture, simulated by a reduction in tendon slack length, were progressively increased for each muscle or muscle group until the simulation failed to replicate unimpaired gait. Kinematic deviations and convergence determined the success of the simulation. The primary outcomes were (1) musculoskeletal impairment thresholds, defined by the amount of weakness or contracture before failure, and (2) neural demand of each gait cycle.Aim: In this study, we use a two-dimensional musculoskeletal model constrained to synergy control to simulate unimpaired gait.

Methods: We vary the number of synergies, while simulating muscle weakness and contracture to examine how altered control impacts sensitivity to musculoskeletal impairment while tracking unimpaired gait.

Results: Results demonstrate that reducing the number of synergies increases sensitivity to weakness and contracture for specific muscle groups. For example, simulations using five-synergy control tolerated 40% and 51% more knee extensor weakness than those using four- or three-synergy control, respectively. Furthermore, when constrained to four- or three-synergy control, the model was increasingly sensitive to contracture and weakness of proximal muscles, such as the hamstring and hip flexors. Contrastingly, neither the amount of generalized nor plantarflexor weakness tolerated was affected by the number of synergies.

Interpretation: These findings highlight the interactions between altered control and musculoskeletal impairments, emphasizing the importance of measuring and incorporating both in future simulation and experimental studies.

N Mehrabi, MH Schwartz, KM Steele (2019) “Can altered muscle synergies control unimpaired gait?” Journal of Biomechanics

Nicole JournalArticle, MotorControl, Publications , , , , ,

Journal Article in Journal of Biomechanics:

Musculoskeletal models of gait with lower dimensional control spaces showed that an individual with reduced number of synergies could not produce an unimpaired gait

Background: 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.

Methods: In this study, using a two-dimensional model of walking, we developed a synergy-based control framework that can simulate the dynamics of walking.

Results: 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.

Conclusions: 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.