Sex Differences in Motor Unit Behavior in Patients With Parkinson's Disease

Abstract

The aim of this study was to determine whether there are sex differences in motor unit firing behavior in patients with Parkinson's disease. Twenty-seven patients with Parkinson's disease (females = 14 [age = 71.1 ± 6.8], males = 13 [age = 69.2 ± 10.3], Unified Parkinson's Disease Rating Scale Part III score; females = 10.8 ± 4.8, males = 11.4 ± 1.4) performed a contraction at 30% of the maximal voluntary contraction. For each participant, motor unit spike trains were decomposed from high-density surface electromyography data recorded from bilateral vastus lateralis muscles via blind source separation algorithms. In addition to the mean discharge rates, persistent inward currents were estimated via a paired motor unit analysis. Females presented significantly greater laterality of discharge rate (p = 0.001) and persistent inward currents (p = 0.0121) than males. A significant correlation was observed between the discharge rate and the recruitment threshold on the bilateral side of males and the less-affected side of females but not on the more-affected side of females. These findings indicate that sex differences in motor unit behavior exist in Parkinson's disease patients. Motor unit behavior may be a sensitive and quantitative evaluation tool to highlight differences in disease presentation between males and females.

Keywords: Parkinson's disease; electromyography; motor unit; sex difference.

FIGURE 1

Study protocol. The participants were seated with their lower distal extremity secured in a device to measure isometric knee extension force, with high‐density surface electromyography electrodes placed on the vastus lateralis muscle (A). During the experiment, two different types of real‐time visual feedback were provided on a monitor in front of the participants (B).

FIGURE 2

Calculation of the persistent inward currents. Example of the calculation of ∆F used to estimate persistent inward currents. ∆F is the test motor unit and is calculated as the mean lower threshold reporter unit change in the discharge rate.

FIGURE 3

Comparison of motor unit discharge characteristics between more‐ and less‐affected sides in male and female patients with Parkinson's disease. (A) CV of ISI. (B) ∆CV of ISI (difference between more‐ and less‐affected sides). (C) Mean discharge rates. (D) ∆ discharge rate (difference between more‐ and less‐affected sides). (E) ∆F values indicating persistent inward currents estimates. (F) ∆∆F (difference between more‐ and less‐affected sides). Data are presented separately for males (left) and females (right). * p < 0.05. Abbreviations: CV of the ISI, coefficient of variation of the interspike interval; pps, pulse per second.

FIGURE 4

Correlations between motor unit parameters and disease severity (UPDRS Part III scores). Panels (A)–(L) show Pearson's correlations for each of the three motor unit indices—CV of the ISI, discharge rate, and ΔF—plotted against UPDRS Part III scores for sex (males/female) and side (more and less affected): Males—more‐affected side: (A) CV of the ISI, (B) discharge rate, and (C) ΔF; males—less‐affected side: (D) CV of the ISI, (E) discharge rate, and (F) ΔF; females—more‐affected side: (G) CV of the ISI, (H) discharge rate, and (I) ΔF; Females—less‐affected side: (J) CV of the ISI, (K) discharge rate, and (L) ΔF. Each dot represents a subject‐average value. Pearson's correlation coefficients (r) and p values are shown within each panel.

FIGURE 5

Relationships between the recruitment threshold and discharge rate across patient groups. (A) Males—more‐affected side, (B) males—less‐affected side, (C) females—more‐affected side, and (D) females—less‐affected side. Locally estimated scatterplot smoothed regression lines are shown in black. Pearson's correlation coefficients (r) and significance levels (p) are indicated in each panel.