Abstract
Cortical oscillatory signals of single and double tremor frequencies act together to cause tremor in the peripheral limbs of patients with Parkinson's disease (PD). But the corticospinal pathway that transmits the tremor signals has not been clarified, and how alternating bursts of antagonistic muscle activations are generated from the cortical oscillatory signals is not well understood. This paper investigates the plausible role of propriospinal neurons (PN) in C3–C4 in transmitting the cortical oscillatory signals to peripheral muscles. Kinematics data and surface electromyogram (EMG) of tremor in forearm were collected from PD patients. A PN network model was constructed based on known neurophysiological connections of PN. The cortical efferent signal of double tremor frequencies were integrated at the PN network, whose outputs drove the muscles of a virtual arm (VA) model to simulate tremor behaviors. The cortical efferent signal of single tremor frequency actuated muscle spindles. By comparing tremor data of PD patients and the results of model simulation, we examined two hypotheses regarding the corticospinal transmission of oscillatory signals in Parkinsonian tremor. Hypothesis I stated that the oscillatory cortical signals were transmitted via the mono-synaptic corticospinal pathways bypassing the PN network. The alternative hypothesis II stated that they were transmitted by way of PN multi-synaptic corticospinal pathway. Simulations indicated that without the PN network, the alternating burst patterns of antagonistic muscle EMGs could not be reliably generated, rejecting the first hypothesis. However, with the PN network, the alternating burst patterns of antagonist EMGs were naturally reproduced under all conditions of cortical oscillations. The results suggest that cortical commands of single and double tremor frequencies are further processed at PN to compute the alternating burst patterns in flexor and extensor muscles, and the neuromuscular dynamics demonstrated a frequency dependent damping on tremor, which may prevent tremor above 8 Hz to occur.
Highlights
Resting tremor in Parkinson’s disease (PD) is elicited by the reciprocal and alternating activities of antagonistic muscles [1]
Simulations without propriospinal neurons (PN) Network Results from the first set of simulations using the CS-virtual arm (VA) model were summarized in Figure 5, in which cortical commands were directly coupled to the motoneuron pools of muscles without the PN network
This result was contradictory to the signature feature of alternating bursts in the flexor and extensor muscles observed in PD patients in Figure 3 and in literature [1], [52,53,54]
Summary
Resting tremor in Parkinson’s disease (PD) is elicited by the reciprocal and alternating activities of antagonistic muscles [1]. The tremor of variable frequency between 3 and 7 Hz is originated from oscillatory neuronal activities in subcortical and cortical networks [2], [3]. All studies revealed that peripheral EMG showed strong coupling with neuronal oscillatory activity in the brain at single tremor frequency and double tremor frequency. A further analysis indicated that the cortical oscillatory activity at double tremor frequency was the main central drive contributing to corticomuscular coupling [11]. The spinal mechanism of corticomuscular processing remains unknown with regard to how the cerebral oscillations of single and double frequencies are transformed into alternating pattern of antagonistic muscle bursts that generate tremor behaviors
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