Coherent Motor Unit Rhythms in the 6–10 Hz Range During Time-Varying Voluntary Muscle Contractions: Neural Mechanism and Relation to Rhythmical Motor Control

Abstract

In quasi-sinusoidal (0.5-3.0 Hz) voluntary muscle contractions, we studied the 6- to 10-Hz motor unit (MU) firing synchrony and muscle force oscillation with emphasis on their neural substrate and relation to rhythmical motor control. Our analyses were performed on data from 121 contractions of a finger muscle in 24 human subjects. They demonstrate that coherent 6- to 10-Hz components of MU discharges coexist with carrier components and coherent modulation components underlying the voluntary force variations. The 6- to 10-Hz synchrony has the frequency of the tremor synchrony in steady contractions and is also widespread and in-phase. Its strength ranges from very small to very large (MU/MU coherence >0.50) among contractions; moreover, it is not related to the contraction parameters, in accord with the notion of a distinct 6- to 10-Hz synaptic input to the MUs. Unlike the coherent MU modulations and the voluntary force variations, the in-phase 6- to 10-Hz MU components are suppressed or even eliminated during ischemia, while the respective force component is drastically reduced. These findings agree with the widely assumed supraspinal origin of the MU modulations, but they also strongly suggest a key role for muscle spindle feedback in the generation of the 6- to 10-Hz synaptic input. They therefore provide important information for the study of generators of the 6- to 10-Hz rhythm which subserves the postulated rhythmical control and is manifested as force and movement components. Moreover, they argue for a participation of oscillating spinal stretch reflex loops in the rhythm generation, possibly in interaction with supraspinal oscillators.

The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback

“…When both muscles are active, these negatively correlated inputs constrain a negative correlation of the output of the two motor neuron populations and accordingly of the muscle forces, implying low steadiness. A similar resonance phenomenon has previously been suggested to cause physiological tremor output (Christakos et al 2006;Erimaki and Christakos 2008;Lippold 1970). As clearly demonstrated by the present results, this motor resonance is dramatically increased when both muscles are active (Fig.…”

“…It has been suggested that a relatively high gain of the Ia input can give rise to undesired resonance in the motor output (Christakos et al 2006;Erimaki and Christakos 2008;Lippold 1970). Such resonance may arise because even a relatively small variability in the output of the motor neurons is always reflected mechanically (Negro et al 2009) and fed back to the motor neurons via afferent pathways (Hagbarth and Young 1979) with a considerable delay.…”

Neuromuscular mechanisms and neural strategies in the control of time-varying muscle contractions

“…In agreement with our previous report using a portion of data set 1 (Erimaki and Christakos 2008), the estimated MU/force coherence at F m varied widely among the 139 contractions and the 154 MUs of the present study (observed range 0.13-0.97), although for each of 13 pairs and 1 triplet of simultaneous MUs it was within 10% of the average value. This coherence was generally high (mean 0.71, SD 0.18), as also seen in Fig.…”

Neural correlates of task-related changes in physiological tremor

“…Overall, task-related changes in antagonist muscle activity and FDI MU recruitment would not clearly explain our findings of altered 7-9 Hz coherence among already-active MUs. In contrast, a change in ongoing afferent feedback would provide an explanation for our results, since 7-to 9-Hz force tremor has been associated with reflex-loop activity and MU-MU coherence in the same range (Elble and Randall 1976;Erimaki and Christakos 2008;Lippold 1970).…”

“…Tremor in this frequency band is associated with the activity of the stretch reflex loop (Christakos et al 2006;Christakos 1999, 2008;Hagbarth and Young 1979;Lippold 1970). Deafferentation can eliminate this tremor (Halliday and Redfearn 1958;Sanes 1985), as can limb ischemia (Erimaki and Christakos 2008); cooling or heating of the forearm changes its frequency, consistent with an influence on conduction delay (Lippold 1970); and common manipulations of stretch-reflex gain change its amplitude (Young and Hagbarth 1980). We found that target-guided contractions produced more 7-9 Hz coherence among MUs than self-guided contractions, which is consistent with the predicted effects of an increase in the magnitude or gain of afferent feedback.…”