Peripheral-central interplay for fatiguing unresisted repetitive movements: a study using muscle ischaemia and M1 neuromodulation

Elena Madinabeitia-Mancebo,Antonio Oliviero,Pablo Arias,Antonio Madrid,Javier Cudeiro

doi:10.1038/s41598-020-80743-x

Abstract

Maximal-rate rhythmic repetitive movements cannot be sustained for very long, even if unresisted. Peripheral and central mechanisms of fatigue, such as the slowing of muscle relaxation and an increase in M1-GABAb inhibition, act alongside the reduction of maximal execution rates. However, maximal muscle force appears unaffected, and it is unknown whether the increased excitability of M1 GABAergic interneurons is an adaptation to the waning of muscle contractility in these movements. Here, we observed increased M1 GABAb inhibition at the end of 30 s of a maximal-rate finger-tapping (FT) task that caused fatigue and muscle slowdown in a sample of 19 healthy participants. The former recovered a few seconds after FT ended, regardless of whether muscle ischaemia was used to keep the muscle slowed down. Therefore, the increased excitability of M1-GABAb circuits does not appear to be mediated by afferent feedback from the muscle. In the same subjects, continuous (inhibitory) and intermittent (excitatory) theta-burst stimulation (TBS) was used to modulate M1 excitability and to understand the underlying central mechanisms within the motor cortex. The effect produced by TBS on M1 excitability did not affect FT performance. We conclude that fatigue during brief, maximal-rate unresisted repetitive movements has supraspinal components, with origins upstream of the motor cortex.

Highlights

Maximal-rate rhythmic repetitive movements cannot be sustained for very long, even if unresisted
Maximal-rate rhythmic repetitive movements (RRMs) cannot be sustained for very long, even when the movements are unresisted, and it is known that the slowing of muscle relaxation is a major peripheral mechanism of RRM fatigue[1,2]
The maximal rate of FT decreased in 30 s ( F1,18 = 153.4, p < 0.001TIME) and the PRE-POST decrement was ≈ 15%

Summary

Introduction

Maximal-rate rhythmic repetitive movements cannot be sustained for very long, even if unresisted. We observed increased M1 GABAb inhibition at the end of 30 s of a maximal-rate finger-tapping (FT) task that caused fatigue and muscle slowdown in a sample of 19 healthy participants The former recovered a few seconds after FT ended, regardless of whether muscle ischaemia was used to keep the muscle slowed down. There is an increase in the concentrations of metabolites (such as H+, ADP, or Pi) and a decrease in ATP turnover, which may cause the contractile properties of the muscle to slow and may simultaneously stimulate different muscle nociceptors and chemoreceptors These receptors (polymodal free nerve endings14,15) give rise to small afferents (type III and IV) that project to different levels of the central nervous s ystem[15,16,17], such as the inhibitory interneurons at the spinal cord[18]. In contrast to resisted repetitive actions such as c ycling[21], unresisted repetitive movements require low levels of muscle force, and the effects of fatigue in these tasks do not compromise central drive to the muscle or muscle force generation, at least for short-duration tasks[8,22]

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Conclusion