Contribution of inter-muscular synchronization in the modulation of tremor intensity in Parkinson's disease

Abstract

Background: Involuntary central oscillations at single and double tremor frequencies drive the peripheral neuromechanical system of muscles and joints to cause tremor in Parkinson's disease (PD). The central signal of double tremor frequency was found to correlate more directly to individual muscle EMGs (Timmermann et al. 2003). This study is aimed at investigating what central components of oscillation contribute to inter-muscular synchronization in a group of upper extremity muscles during tremor in PD patients.

Methods: 11 idiopathic, tremor dominant PD subjects participated in this study. Joint kinematics during tremor in the upper extremity was recorded along with EMGs of six upper arm muscles using a novel experimental apparatus. The apparatus provided support for the upper extremity on a horizontal surface with reduced friction, so that resting tremor in the arm can be recorded with a MotionMonitor II system. In each subject, the frequencies of rhythmic firings in upper arm muscles were determined using spectral analysis. Paired and pool-averaged coherence analyses of EMGs for the group of muscles were performed to correlate the level of inter-muscular synchronization to tremor amplitudes at shoulder and elbow. The phase shift between synchronized antagonistic muscle pairs was calculated to aid coherence analysis in the muscle pool.

Results: Recorded EMG revealed that rhythmic firings were present in most recorded muscles, which were either synchronized to form phase-locked bursting cycles at a subject specific frequency, or unsynchronized with a random phase distribution. Paired coherence showed a stronger synchronization among a subset of recorded arm muscles at tremor frequency than that at double tremor frequency. Furthermore, the number of synchronized muscles in the arm was positively correlated to tremor amplitudes at elbow and shoulder. Pool-averaged coherence at tremor frequency also showed a better correlation with the amplitude of resting tremor than that of double tremor frequency, indicating that the neuromechanical coupling in peripheral neuromuscular system was stronger at tremor frequency.

Conclusions: Both paired and pool-averaged coherences are more consistent indexes to correlate to tremor intensity in a group of upper extremity muscles of PD patients. The central drive at tremor frequency contributes mainly to synchronize peripheral muscles in the modulation of tremor intensity.

Fig. 1

The experimental setup for Parkinsonian tremor recording. Six channels of surface electromyography (sEMG) were recorded from each subject by placing bipolar sEMG electrodes on top of muscles that exhibited evident involuntary oscillatory activities in the upper extremity. Joint movements were tracked by magnetic motion sensors attached to body segments in a gradient magnetic field generated by the magnetic transmitter. The cast apparatus with magnetic compatible design can provide antigravity support for the arm without affecting tremor behaviors by introducing significant damping and friction effects

Fig. 2

The sEMG and joint angle trajectory during Parkinsonian tremor recorded from PD subject P9. a The sEMG of 6 muscles are shown in the left column, and the corresponding spectra are shown in the right column. The EMGs show similar rhythms of spontaneous oscillatory activities across all muscles, and all the spectra show similar two major components at single and double tremor frequencies. b Oscillations in elbow (flexion) and shoulder (flexion, abduction, and rotation) joints are demonstrated in the left column, and the corresponding spectra are presented in the right column. Joint trajectory spectra show a single component at the tremor frequency

Fig. 3

Coherence analyses for evaluation of inter-muscular synchronization. a The paired coherence between muscles FDS and ED in subject P9. The horizontal red line indicates the 99 % upper confidence limit of significant coherence level. The vertical green lines indicate the subject-specific tremor frequency and double tremor frequency of subject P9. b The pooled coherence of all 15 pairs of muscles among 6 recorded muscles in subject P9. The horizontal red line indicates the 99 % upper confidence limit of significant coherence level. c The pool-averaged coherence of all 15 pairs among 6 recorded muscles in subject P9

Fig. 4

The characteristic tremor frequencies detected from muscle EMGs of 11 PD subjects. For each subject, 6 muscles exhibited significant tremor activities out of the following 8 muscles are recorded: FDS (flexor digitorum superficialis), ED (extensor digitorum), FCR (flexor carpi radialis), ECR (extensor carpi radialis), FCU (flexor carpi ulnaris), Biceps, Triceps, and DA (deltoid anterior). Muscles revealed detectable oscillation frequency are listed as bars (error bars: standard deviation) in this figure, and the resultant F-statistic (F_DF, in which DF denotes the degrees of freedom) and P-value in the one-way ANOVA of each subject are listed above. The one-way ANOVA test results indicate that there is no significant difference among EMG tremor frequencies of recorded muscles in each subject except P7 (indicated by ‘*’). The subject-specific tremor frequency (red diamond) is averaged from all EMG tremor frequencies of each subject, and the standard deviations of EMG tremor frequencies are given as error bars

Fig. 5

The correlations between different estimates of inter-muscular synchronization. a Linear regression between the number of synchronized muscles and the pooled coherence / pool-averaged coherence level at tremor frequency detected from each subject. The pool-averaged coherence at tremor frequency shows fine linear relationship with the number of synchronized muscles, while the pooled coherence doesn’t. b Linear regression between the number of synchronized muscles and the pooled coherence / pool-averaged coherence level at double tremor frequency. The pool-averaged coherence at double tremor frequency also shows significant linear relationship with the number of synchronized muscles, while the pooled coherence doesn’t

Fig. 6

The relationship between the number of synchronized muscles and the tremor amplitudes in shoulder and elbow joints in PD subjects. The correlations between tremor amplitudes in a elbow flexion, b shoulder flexion, c shoulder abduction, and d shoulder rotation and the number of synchronized muscles are evaluated by exponential regression. Different subjects are indicated with different markers and the error bars indicate the standard deviation of tremor amplitudes of each subject. The R² (squared correlation coefficients) and P values are given in the figure. Tremor amplitudes in joints are strongly correlated with the number of synchronized muscles except for shoulder flexion that shows only a mild correlation

Fig. 7

Correlations between the pool-averaged coherence levels at tremor frequency and the tremor amplitudes in shoulder and elbow joints. Exponential regression results show that the tremor amplitudes in DOFs of a elbow flexion, c shoulder abduction, and d shoulder rotation are significantly correlated with the pool-averaged coherence level at tremor frequency, while that of b shoulder flexion isn’t. Different subjects are indicated with different markers and the error bars indicate the standard deviation of tremor amplitudes of each subject

Fig. 8

Correlations between the pool-averaged coherence levels at double tremor frequency and the tremor amplitudes in shoulder and elbow joints. Exponential regression results show that the tremor amplitudes in DOFs of a elbow flexion, b shoulder flexion, c shoulder abduction, and d shoulder rotation are not significantly correlated with the pool-averaged coherence level at double tremor frequency. Different subjects are indicated with different markers and the error bars indicate the standard deviation of tremor amplitudes of each subject

Fig. 9

The phase shift between 3 pairs of antagonistic muscles averaged from all PD subjects. The error bars indicate the standard deviation of phase shift calculated from all subjects