Abstract
Pathological tremor is an oscillation of body parts at 3–10 Hz, determined by the output of spinal motor neurons (MNs), which receive synaptic inputs from supraspinal centers and muscle afferents. The behavior of spinal MNs during tremor is not well understood, especially in relation to the activation of the multiple muscles involved. Recent studies on patients with essential tremor have shown that antagonist MN pools receive shared input at the tremor frequency. In this study, we investigated the synaptic inputs related to tremor and voluntary movement, and their coordination across antagonist muscles. We analyzed the spike trains of motor units (MUs) identified from high-density surface electromyography from the forearm extensor and flexor muscles in 15 patients with essential tremor during postural tremor. The shared synaptic input was quantified by coherence and phase difference analysis of the spike trains. All pairs of spike trains in each muscle showed coherence peaks at the voluntary drive frequency (1–3 Hz, 0.2 ± 0.2, mean ± SD) and tremor frequency (3–10 Hz, 0.6 ± 0.3) and were synchronized with small phase differences (3.3 ± 25.2° and 3.9 ± 22.0° for the voluntary drive and tremor frequencies, respectively). The coherence between MN spike trains of antagonist muscle groups at the tremor frequency was significantly smaller than intramuscular coherence. We predominantly observed in-phase activation of MUs between agonist/antagonist muscles at the voluntary frequency band (0.6 ± 48.8°) and out-of-phase activation at the tremor frequency band (126.9 ± 75.6°). Thus MNs innervating agonist/antagonist muscles concurrently receive synaptic inputs with different phase shifts in the voluntary and tremor frequency bands.NEW & NOTEWORTHY Although the mechanical characteristics of tremor have been widely studied, the activation of the affected muscles is still poorly understood. We analyzed the behavior of motor units of pairs of antagonistic wrist muscle groups in patients with essential tremor and studied their activity at voluntary movement- and tremor-related frequencies. We found that the phase relation between inputs to antagonistic muscles is different at the voluntary and tremor frequency bands.
Highlights
Tremor is characterized by rhythmic oscillations of body parts around joints (Lyons and Pahwa 2005)
The total number of motor unit (MU) spike trains that were analyzed from the 15 subjects was 211 (6.8 Ϯ 4.0 MUs per muscle group)
In most patients (11 of 15), the MUs in at least one group of muscles showed a power peak at the voluntary drive frequency, and in 5 of 31 cases, the peak of the power spectrum at the voluntary drive frequency was higher than the peak at the tremor frequency
Summary
Tremor is characterized by rhythmic oscillations of body parts around joints (Lyons and Pahwa 2005). It is suggested that tremor originates from abnormal oscillations in supraspinal centers, such as in the cerebello-thalamo-cortical pathway (Benito-León and Louis 2006), potentially involving the basal ganglia (Louis 2005; Lyons and Pahwa 2005) and motor cortex, as well (Gallego et al 2015b; Raethjen et al 2007) These pathological neural oscillations may be amplified or attenuated by “resonance” due to the limb properties and the reflex loops (Deuschl et al 2001; Gallego et al 2015b; Lakie et al 2012). The contributions of these feedback components to tremor severity are largely unknown
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