Parallel Neuronal Mechanisms Underlying Physiological Force Tremor in Steady Muscle Contractions of Humans

Abstract

We present results from a study of the 6-to 12-Hz force tremor in relation to motor unit (MU) firing synchrony. Our experimental observations from 32 subjects, 321 contractions, and 427 recorded MUs reveal that tremor is accompanied by corresponding, in-phase MU rhythms that are additional to the ones at the MU intrinsic firing rates. This rhythmical synchrony is widespread and has a uniform strength that ranges from near zero to very large (MU/MU coherence > 0.50) in different contractions. Both the synchrony and the tremor are suppressed during ischemia, and this strongly suggests an involvement of spindle feedback in their generation. Furthermore, in the presence of substantial synchrony, the tremor enhancement, relative to the minimal tremor of ischemia, reflects the strength of the synchrony. Theoretical considerations based on these observations indicate that the muscle force signal is expected to show 1) frequency components in the band of the firing rates of the last-recruited, large MUs, and 2) because of the synchronized MU rhythms, an additional, distinct component with a size reflecting the strength of synchrony. Furthermore, synchronized MU rhythms, with frequencies in the 6- to 12-Hz range, are expected to arise from self-oscillations in the monosynaptic stretch reflex loop, due primarily to the associated muscle delay (several tens of milliseconds). Our results therefore reveal the parallel action of two tremor mechanisms, one of which involves MU synchrony probably caused by loop action. Clearly, the results on the synchrony and its impact also apply to other possible generators of tremor synchrony, including supraspinal ones.

Bilateral motor unit synchronization is functionally organized

“…That is, rhythmic MU synchronization, e.g., underlying tremor activity, reXects in-phase MU rhythms that are additional to those at the MU intrinsic Wring rates (cf. Christakos et al 2006). Put diVerently, there is not necessarily an entrapment of the Wring rates of individual MUs into the 8-12 Hz rhythm, but MU synchronization, as measured by surface EMG, reXects rhythmic modulation of the total EMG amplitude and suggests rhythmic input.…”

10 Hz periodic component influences lower frequency component of the physiological tremor at low force levels

“…It has also been shown that there are several frequency peaks in the PT (Christakos et al 2006;Elble 1996;Halliday et al 1999;McAuley and Marsden 2000;McAuley et al 1997;Takanokura and Sakamoto 2001;Vaillancourt and Newell 2000). For example, finger tremors show oscillations at 10, 20, and 40 Hz (McAuley et al 1997;Takanokura and Sakamoto 2001;Vaillancourt and Newell 2000).…”

“…These fluctuations, observed in normal individuals, are known as the physiological tremor (PT). Though fluctuation amplitude has been shown to correlate positively with muscle force (Moritz et al 2005;Taylor et al 2003), the amplitude in the frequency domain is more damped at higher frequencies (Christakos et al 2006;Erimaki and Christakos 1999;Sowman and Türker 2005;Taylor et al 2003). For example, the amplitude of finger force fluctuation was shown to fall off at approximately −30 dB/decade in the squared power spectrum around 10 Hz (approximately between 1 and 30 Hz) (Allum et al 1978;Endo and Kawahara 2010).…”

“…The 10-Hz component is the most common frequency peak in neurophysiologic tremors, which are associated with peaks ranging between 6 Hz and 12 Hz (Christakos et al 2006;Elble 1996;McAuley and Marsden 2000). The 20-Hz component of finger tremors is due to oscillations caused by mechanical resonance observed in postural tremors.…”

“…The 40-Hz component is also neurological but cannot always be detected clearly (McAuley et al 1997). During a force-holding task, the frequency peak around 10 Hz is often observed in the power spectrum of fluctuations (Christakos et al 2006;Elble and Randall 1976;McAuley and Marsden 2000;McAuley et al 1997;Nordstrom 1995, 1998). To sum up, the fluctuation that is composed of low frequency components is the dominant component of force tremors, and the fluctuation that oscillates around 10 Hz appears as a second prominent component.…”