Abstract

Spinal interneurons are partially phase-locked to physiological tremor around 10 Hz. The phase of spinal interneuron activity is approximately opposite to descending drive to motoneurons, leading to partial phase cancellation and tremor reduction. Pre-synaptic inhibition of afferent feedback modulates during voluntary movements, but it is not known whether it tracks more rapid fluctuations in motor output such as during tremor. In this study, dorsal root potentials (DRPs) were recorded from the C8 and T1 roots in two macaque monkeys following intra-spinal micro-stimulation (random inter-stimulus interval 1.5–2.5 s, 30–100 μA), whilst the animals performed an index finger flexion task which elicited peripheral oscillations around 10 Hz. Forty one responses were identified with latency < 5 ms; these were narrow (mean width 0.59 ms), and likely resulted from antidromic activation of afferents following stimulation near terminals. Significant modulation during task performance occurred in 16/41 responses, reflecting terminal excitability changes generated by pre-synaptic inhibition (Wall's excitability test). Stimuli falling during large-amplitude 8–12 Hz oscillations in finger acceleration were extracted, and sub-averages of DRPs constructed for stimuli delivered at different oscillation phases. Although some apparent phase-dependent modulation was seen, this was not above the level expected by chance. We conclude that, although terminal excitability reflecting pre-synaptic inhibition of afferents modulates over the timescale of a voluntary movement, it does not follow more rapid changes in motor output. This suggests that pre-synaptic inhibition is not part of the spinal systems for tremor reduction described previously, and that it plays a role in overall—but not moment-by-moment—regulation of feedback gain.

Highlights

  • Physiological tremor is produced by multiple interacting mechanisms

  • In this work we have provided evidence that pre-synaptic inhibition does not show moment-by-moment modulation with the phase of physiological tremor, by contrast it does modulate on the slower timescales of behavioral task performance

  • We propose that the narrow, early responses seen in the dorsal root potentials (DRPs) were probably generated by antidromic action potentials following stimulation of afferent axons within the spinal cord

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Summary

INTRODUCTION

Physiological tremor is produced by multiple interacting mechanisms. These include mechanical resonance of limb articulations (Marsden et al, 1969), and oscillations in the stretch reflex loop consequent on the peripheral conduction delays (Lippold, 1970). If the phase of such modulation were appropriate, this could lead to partial cancelation of oscillations in afferent activity, smoothing out the peaks and troughs and reducing the afferent contribution to tremor amplitude Such a timescale of modulation of presynaptic inhibition would be an order of magnitude faster than that reported previously during task performance in awake animals. Robust modulation over the second-to-second timescale of task performance was regularly seen, the data contained no evidence for faster modulation during the tremor cycle These results suggest that pre-synaptic inhibition may act as a less temporally-precise gate for afferent inflow, but does not sculpt sensory input and its reflex consequences over timescales comparable to endogenous oscillations in motor output

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