Muscle shape changes in Parkinson's disease impair function during rapid contractions

Abstract

Aim: Parkinson's disease (PD) is a progressive neurodegenerative disorder characterized, among the others, by muscle weakness. PD patients reach lower values of peak torque during maximal voluntary contractions but also slower rates of torque development (RTD) during explosive contractions. The aim of this study was to better understand how an impairment in structural/mechanical (peripheral) factors could explain the difficulty of PD patients to raise torque rapidly. Methods: Participants (PD patients and healthy matched controls) performed maximum voluntary explosive fixed-end contraction of the knee extensor muscles during which dynamic muscle shape changes (in muscle thickness, pennation angle, and belly gearing: the ratio between muscle belly velocity and fascicle velocity), muscle-tendon unit (MTU) stiffness and EMG activity of the vastus lateralis (VL) were investigated. Both the affected (PDA) and less affected limb (PDNA) were investigated in patients.Results: Control participants reached higher values of peak torque and showed a better capacity to express force rapidly compared to patients (PDA and PDNA). EMG activity was observed to differ between patients (PDA) and controls, but not between controls and PDNA. This suggests a specific neural/nervous effect on the most affected side. On the contrary, MTU stiffness and dynamic muscle shape changes were found to differ between controls and patients, but not between PDA and PDNA. Both sides are thus similarly affected by the pathology. Conclusion:The higher MTU stiffness in PD patients is likely responsible for the impaired muscle capability to change in shape which, in turn, negatively affects the torque rise.

Characterization of the vastus lateralis torque-length, and knee extensors torque-velocity and power-velocity relationships in people with Parkinson's disease

“…In this regard, from a neural/nervous point of view, a lower EMG amplitude during maximum explosive contractions was observed in PD patients compared to healthy age-matched control participants ( 13 , 15 ). Furthermore, PD patients exhibit higher antagonist co-activation ( 16 ) and variable motor unit discharge rates ( 17 ) during maximal and submaximal isometric force reduction compared to healthy subjects, which in turn decrease force production capacity ( 18 ).…”

“…Resting muscle geometry was observed to be similar between PD patients and age and physically-matched control groups ( 13 , 15 ) whereas fascicle and muscle behaviour were found to differ in dynamic conditions (e.g., during explosive contractions; ( 13 ). Indeed, PD patients showed higher values of MTU stiffness during contraction compared to healthy controls reducing the muscle's capability to change in shape and to increase force production rapidly ( 13 ).…”

“…Resting muscle geometry was observed to be similar between PD patients and age and physically-matched control groups ( 13 , 15 ) whereas fascicle and muscle behaviour were found to differ in dynamic conditions (e.g., during explosive contractions; ( 13 ). Indeed, PD patients showed higher values of MTU stiffness during contraction compared to healthy controls reducing the muscle's capability to change in shape and to increase force production rapidly ( 13 ). Therefore, the concomitant evaluation of muscle geometry at rest and during contraction, as well as that of the torque-length and power-velocity relationships, could represent an important screening for people with PD, providing information about the level/progression of this pathology.…”

“…The decrease in functional performance observed in patients with Parkinson's disease (PD) can be attributed to various factors, one of which is muscle weakness ( 8 ). This weakness is linked to both central and peripheral alterations, such as a decrease in voluntary activation ( 9 ), altered spatial activation pattern ( 10 ), diminished fascicle shortening and tendon elongation ( 11 ), increased muscle stiffness ( 12 ) and decreased muscle's capability to change in shape ( 13 ). Although the effects of the central parameters in determining the loss of force in people with PD are well acknowledged in the literature [e.g., ( 14 , 15 )], the impact of peripheral variables remains unclear.…”

The role of pennation angle and architectural gearing to rate of force development in dynamic and isometric muscle contractions

“…13,22 The architectural gear ratio has been shown to be >1.0 under various contraction conditions in both animal 20,23,24 and human experiments, 10,25,26 although the magnitude of effect depends on the requirements of the task such as the force produced 20,26,27 (Figure 1) and the rate at which force is produced. 28 Furthermore, the gear ratio also depends on the spacing between fascicles 27 and material characteristics of the muscle-tendon unit such as the stiffness of connective tissues (i.e., extracellular matrix and aponeurosis 23,28,29 ), where higher connective tissue stiffness may restrict the muscle's capability to change in shape. Similarly, because longer tendons are more compliant than shorter tendons if cross-sectional area and material properties are similar (e.g., ref.…”