Spinal interneuron circuits reduce approximately 10-Hz movement discontinuities by phase cancellation

Abstract

Tremor imposes an important limit to the accuracy of fine movements in healthy individuals and can be a disabling feature of neurological disease. Voluntary slow finger movements are not smooth but are characterized by large discontinuities (i.e., steps) in the tremor frequency range (approximately 10 Hz). Previous studies have shown that these discontinuities are coherent with activity in the primary motor cortex (M1), but that other brain areas are probably also involved. We investigated the contribution of three important subcortical areas in two macaque monkeys trained to perform slow finger movements. Local field potential and singleunit activity were recorded from the deep cerebellar nuclei (DCN), medial pontomedullary reticular formation, and the intermediate zone of the spinal cord (SC). Coherence between LFP and acceleration was significant at 6 to 13 Hz for all areas, confirming the highly distributed nature of the central network responsible for this activity. The coherence phase at 6 to 13 Hz for DCN and pontomedullary reticular formation was similar to our previous results in M1. By contrast, for SC the phase differed from M1 by approximately π rad. Examination of single-unit discharge confirmed that this was a genuine difference in neural spiking and could not be explained by different properties of the local field potential. Convergence of antiphase oscillations from the SC with cortical and subcortical descending inputs will lead to cancellation of approximately 10 Hz oscillations at the motoneuronal level. This could appreciably limit drive to muscle at this frequency, thereby reducing tremor and improving movement precision.T remor is a key limitation to human fine motor performance.However, in tremor research, the puzzle is not so much why our hands shake, but why they often do not. Numerous mechanisms can contribute to unstable contraction: motoneurons are recruited at a fixed frequency, limb segments have mechanical resonance, the monosynaptic stretch reflex arc can produce feedback oscillations, and there are a plethora of central neural oscillators. These factors often converge to produce mechanical oscillations at approximately 10 Hz, the dominant frequency of physiological tremor. Yet despite these multiple sources of instability, in most people, most of the time, tremor is small enough not to impact daily life. We have hypothesized that a specific neural system might have evolved to reduce tremor (1), with clear survival advantages.Slow finger movements in man are characterized by steps or discontinuities that occur at approximately 10 Hz (2). These discontinuities provide a good model for studying tremor, as even though they occur within the same frequency range, they are an order of magnitude bigger (2), facilitating quantitative analysis. Work on both physiological tremor and slow finger movement discontinuities has shown that there is an approximately 10

Analysis of the effects of mechanically induced tremor on EEG-EMG coherence using wavelet and partial directed coherence

“…Oscillations in the alpha (8)(9)(10)(11)(12) and beta (13-35 Hz) frequency band are commonly observed in recordings from the primary motor cortex [1]. Similar oscillations can also be detected in the electromyogram (EMG) of forearm and intrinsic hand muscles during sustained contraction.…”

Improved Sensorimotor Performance via Stochastic Resonance

“…However, this is quite unlikely as the stochastic nature of the noise makes it impossible to synchronize in antiphase the tremor oscillations. Another possible explanation for the better performance during ON is the suppression or reduction of the physiological tremor by supraspinal centers shown to be involved in the generation of 10 Hz tremor, such as the pontomedullary reticular formation and the deep cerebellar nuclei (Williams and Baker, 2009;Williams et al, 2010). These authors reported in monkeys that these supraspinal centers exhibit oscillations in neuronal activity at a tremor frequency occurring in antiphase with the oscillations generated by the spinal interneuron circuits.…”

Decorrelation of cortical inputs and motoneuron output

“…Similarly to the first issue discussed, this also implies that the secondary input may not be completely independent from the cortical inputs to the motoneuron pool, at least for the lower frequencies (approximately up to 10 Hz). The problem was investigated recently (Williams et al 2010;Tetzlaff et al 2010), and the results showed that an (inhibitory) feedback to a motoneuron pool can decrease the power of the oscillatory activity present in those frequency ranges and therefore affect the transmission of those frequencies.…”

“…This interaction may act as neural filtering by suppressing or enhancing specific frequency components in the neural drive to muscles (motoneuron output) (Williams et al 2010). These mechanisms are relevant for force stability and may cause pathological conditions when the neural filtering is not fully effective, e.g., in pathological tremor (Halliday et al 1995;Raethjen et al 2009).…”