Non-neural Muscle Weakness Has Limited Influence on Complexity of Motor Control during Gait.

Marije Goudriaan,Guy Molenaers,Marleen Van Den Hauwe,Kaat Desloovere,Nathalie Goemans,Katherine M Steele,Benjamin R Shuman

doi:10.3389/fnhum.2018.00005

Marije Goudriaan, Guy Molenaers + Show 5 more

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https://doi.org/10.3389/fnhum.2018.00005

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Abstract

Cerebral palsy (CP) and Duchenne muscular dystrophy (DMD) are neuromuscular disorders characterized by muscle weakness. Weakness in CP has neural and non-neural components, whereas in DMD, weakness can be considered as a predominantly non-neural problem. Despite the different underlying causes, weakness is a constraint for the central nervous system when controlling gait. CP demonstrates decreased complexity of motor control during gait from muscle synergy analysis, which is reflected by a higher total variance accounted for by one synergy (tVAF1). However, it remains unclear if weakness directly contributes to higher tVAF1 in CP, or whether altered tVAF1 reflects mainly neural impairments. If muscle weakness directly contributes to higher tVAF1, then tVAF1 should also be increased in DMD. To examine the etiology of increased tVAF1, muscle activity data of gluteus medius, rectus femoris, medial hamstrings, medial gastrocnemius, and tibialis anterior were measured at self-selected walking speed, and strength data from knee extensors, knee flexors, dorsiflexors and plantar flexors, were analyzed in 15 children with CP [median (IQR) age: 8.9 (2.2)], 15 boys with DMD [8.7 (3.1)], and 15 typical developing (TD) children [8.6 (2.7)]. We computed tVAF1 from 10 concatenated steps with non-negative matrix factorization, and compared tVAF1 between the three groups with a Mann-Whiney U-test. Spearman's rank correlation coefficients were used to determine if weakness in specific muscle groups contributed to altered tVAF1. No significant differences in tVAF1 were found between DMD [tVAF1: 0.60 (0.07)] and TD children [0.65 (0.07)], while tVAF1 was significantly higher in CP [(0.74 (0.09)] than in the other groups (both p < 0.005). In CP, weakness in the plantar flexors was related to higher tVAF1 (r = −0.72). In DMD, knee extensor weakness related to increased tVAF1 (r = −0.50). These results suggest that the non-neural weakness in DMD had limited influence on complexity of motor control during gait and that the higher tVAF1 in children with CP is mainly related to neural impairments caused by the brain lesion.

Highlights

Two of the most common neurological and neuromuscular diseases in childhood are cerebral palsy (CP) and Duchenne muscular dystrophy (DMD) (Sussman, 2002; Rosenbaum et al, 2007; Graham et al, 2016)
The tVAF1 was significantly higher in the children with CP compared to DMD and typical developing (TD) children
No significant differences in tVAF1 were found between the boys with DMD and the TD children

Summary

Introduction

Two of the most common neurological and neuromuscular diseases in childhood are cerebral palsy (CP) and Duchenne muscular dystrophy (DMD) (Sussman, 2002; Rosenbaum et al, 2007; Graham et al, 2016). Lack of dystrophin in muscles leads to a disbalance between damage and repair of the muscle fibers (Kobayashi and Campbell, 2012). This damage results in muscles that predominantly consist of fat and fibrous tissue (Sussman, 2002; Jones et al, 2010). CP and DMD have different origins and expressions, they have at least one symptom in common: muscle weakness In both groups, muscle weakness is considered an important contributor to their pathological gait patterns (Sutherland et al, 1981; D’Angelo et al, 2009; Gage et al, 2009; Gaudreault et al, 2010; Doglio et al, 2011; Ganea et al, 2012; Steele et al, 2012)

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