Number of Synergies Impacts Sensitivity of Gait to Weakness and Contracture

Muscle activity during gait can be described by a small set of synergies, weighted groups of muscles, that are often theorized to reflect underlying neural control. For people with neurologic injuries, like in cerebral palsy or stroke, even fewer (e.g., < 5) synergies are required to explain muscle activity during gait. This reduction in synergies is thought to reflect simplified control strategies and is associated with impairment severity and treatment outcomes. Individuals with neurologic injuries also develop secondary musculoskeletal impairments, like weakness or contracture, that can also impact gait. The combined impacts of simplified control and musculoskeletal impairments on gait remains unclear. In this study, we use a musculoskeletal model constrained to synergies to simulate unimpaired gait. We vary the number of synergies (3-5), while simulating muscle weakness and contracture to examine how altered control impacts sensitivity to muscle weakness and contracture. Our results highlight that reducing the number of synergies increases sensitivity to weakness and contracture. For example, simulations using five-synergy control tolerated 40% and 51% more knee extensor weakness than those using four- and three-synergy control, respectively. Furthermore, the model became increasingly sensitive to contracture and proximal muscle weakness, such as hamstring and hip flexor weakness, when constrained to four- and three-synergy control. However, the model’s sensitivity to weakness of the plantarflexors and smaller bi-articular muscles was not affected by the number of synergies. These findings provide insight into the interactions between altered control and musculoskeletal impairments, emphasizing the importance of incorporating both in future simulation studies.


38
Muscle synergy analysis decomposes muscle excitations to identify common patterns of co-39 activation during dynamic activities. These patterns are theorized to reflect modular spinal and 40 supraspinal networks that are used to control movement (Kargo et al., 2010;Stein, 2008) and 41 reduce the dimensionality of neuromuscular control (Tresch and Jarc, 2009). More recently, weakness, contracture, and reliance on fewer synergies, make achieving a typical gait pattern 59 more difficult. However, these impairments were imposed in isolation; therefore, not addressing 60 4 if altered control inhibits adaptation to musculoskeletal impairments (Fox et al., 2018). A 61 previous simulation study examined the combined effects of these impairments in the presence 62 of aberrant musculoskeletal geometries. Results highlighted that the number of synergies may 63 influence how musculoskeletal impairments impact gait and suggested that altered muscle-64 tendon properties, rather than impaired motor control, were the primary cause of abnormal gait in 65 a case study of a child with CP (Falisse et al., 2020).

66
The purpose of the present study was to examine the interactions between neuromuscular and 67 musculoskeletal impairments on unimpaired gait. Specifically, we used musculoskeletal 68 simulation to examine how the number of synergies controlling movement alters the sensitivity 69 of unimpaired gait to weakness and contracture. We used a direct collocation framework   79 We built a sagittal plane, musculoskeletal model based on the planar model of (Geyer and Herr, 80 2010) and added the rectus femoris similar to (Dorn et al., 2015) in MapleSim (Maplesoft, Inc).

81
The model consisted of seven rigid body segments -one combined head, arms, and torso (HAT)

158
We progressively increased weakness or contracture, using 1% increments for weakness and 159 0.1% increments for contracture, until the simulation failed to replicate unimpaired gait. Points

196
The weakness thresholds for specific muscle groups varied. We deemed muscle groups control

246
The sensitivity of neural demand to weakness increased as the control strategy used fewer 247 synergies for most muscles (Figure 4c). The quadratic fit comparing the difference in neural 248 demand between three-and five-synergy control was 3.5x that of four-synergy control. That is, 249 as weakness progressed, the neural demand of three-synergy control increased and deviated from 250 baseline control more rapidly than four-synergy control. For example, when ALL muscles were were less influential on neural demand for the control insensitive muscles, with GAS, GLU, and 255 RF second-order coefficients close to zero.

256
The sensitivity of neural demand to contracture increased as the control strategy used fewer 257 synergies ( Figure 5). When averaged across the contracture scenarios, the second-order 258 coefficient was 2.5x larger for three-than four-synergy control. Deviations from five-synergy 259 control, as measured by the average second-order coefficient between four-and three-synergy 260 control, were largest for contracture of the plantarflexors (SOL, GAS, and SOL + GAS) and 261 smallest for HAM contracture.

267
This study found that impaired motor control (e.g., a control strategy constrained to fewer 268 synergies) impacts how sensitive unimpaired gait is to musculoskeletal impairments. This properties.

316
The neural demand of unimpaired gait was most sensitive to total body and plantarflexor 317 weakness and plantarflexor contracture, aligning with previous results indicating that 318 impairments in these muscle groups lead to large increases in neural demand ( There are no conflicts of interest to report.