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

He X, Hao MZ, Wei M, Xiao Q, Lan N - J Neuroeng Rehabil (2015)

Bottom Line: In each subject, the frequencies of rhythmic firings in upper arm muscles were determined using spectral analysis.The phase shift between synchronized antagonistic muscle pairs was calculated to aid coherence analysis in the muscle pool.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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Rehabilitation Engineering, Med-X Research Institute and School of Biomedical Engineering, Shanghai Jiao Tong University, 1954 Hua Shan Road, Shanghai, 200030, China.

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.

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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
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Fig9: 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

Mentions: One interesting finding in this study is that the synchronization between muscles at tremor frequency is always stronger than that at double tremor frequency (Fig. 5). Furthermore, the pool-averaged coherence at tremor frequency (Fig. 7) is more strongly correlated to tremor amplitude than that at double tremor frequency (Fig. 8). Thus muscles are inter-coupled more strongly at tremor frequency than at double tremor frequency in the periphery. This is in contrast to the finding that the oscillations in cortical and sub-cortical areas showed a more preeminent coupling at double tremor frequency [14]. It suggests that between the two central driving signals oscillating at single tremor and double tremor frequencies, the signal at single tremor frequency tends to synchronize the muscles, while the signal at double tremor frequency provides a direct drive to the muscles [14]. The results further imply that a change in frequency content has taken place during corticospinal transmission of tremor signals. Hao et al. [27] proposed a corticospinal mechanism of tremor signal transmission, and described the process within the propriospinal neuron (PN) network, where an alternating pattern of antagonistic muscle activation is generated from the pair of central oscillation signals. The central oscillation at double tremor frequency is gated at the PN network by the signal with tremor frequency to produce alternating bursts at tremor frequency that drive a pair of antagonistic muscles. This PN processing consequently converts the central tremor signal with dominant double tremor frequency to single tremor frequency in the peripheral muscles, and translates frequency contents to give rise to a more favorable condition for tremor to occur in the periphery. This favorable condition is manifested in the near half-cycle phase shift between synchronized antagonistic muscles [12, 43, 44], which was 191.6° ± 40.9° in the subjects (Fig. 9).Fig. 9


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

He X, Hao MZ, Wei M, Xiao Q, Lan N - J Neuroeng Rehabil (2015)

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
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4666195&req=5

Fig9: 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
Mentions: One interesting finding in this study is that the synchronization between muscles at tremor frequency is always stronger than that at double tremor frequency (Fig. 5). Furthermore, the pool-averaged coherence at tremor frequency (Fig. 7) is more strongly correlated to tremor amplitude than that at double tremor frequency (Fig. 8). Thus muscles are inter-coupled more strongly at tremor frequency than at double tremor frequency in the periphery. This is in contrast to the finding that the oscillations in cortical and sub-cortical areas showed a more preeminent coupling at double tremor frequency [14]. It suggests that between the two central driving signals oscillating at single tremor and double tremor frequencies, the signal at single tremor frequency tends to synchronize the muscles, while the signal at double tremor frequency provides a direct drive to the muscles [14]. The results further imply that a change in frequency content has taken place during corticospinal transmission of tremor signals. Hao et al. [27] proposed a corticospinal mechanism of tremor signal transmission, and described the process within the propriospinal neuron (PN) network, where an alternating pattern of antagonistic muscle activation is generated from the pair of central oscillation signals. The central oscillation at double tremor frequency is gated at the PN network by the signal with tremor frequency to produce alternating bursts at tremor frequency that drive a pair of antagonistic muscles. This PN processing consequently converts the central tremor signal with dominant double tremor frequency to single tremor frequency in the peripheral muscles, and translates frequency contents to give rise to a more favorable condition for tremor to occur in the periphery. This favorable condition is manifested in the near half-cycle phase shift between synchronized antagonistic muscles [12, 43, 44], which was 191.6° ± 40.9° in the subjects (Fig. 9).Fig. 9

Bottom Line: In each subject, the frequencies of rhythmic firings in upper arm muscles were determined using spectral analysis.The phase shift between synchronized antagonistic muscle pairs was calculated to aid coherence analysis in the muscle pool.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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Rehabilitation Engineering, Med-X Research Institute and School of Biomedical Engineering, Shanghai Jiao Tong University, 1954 Hua Shan Road, Shanghai, 200030, China.

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.

Show MeSH
Related in: MedlinePlus