Locomotor-like leg movements evoked by rhythmic arm movements in humans.

Francesca Sylos-Labini,Germana Cappellini,Francesco Lacquaniti,Michael J Maclellan,Richard E Poppele,Yuri P Ivanenko,Robert J Van Beers

doi:10.1371/journal.pone.0090775

Francesca Sylos-Labini, Germana Cappellini + Show 5 more

Open Access

https://doi.org/10.1371/journal.pone.0090775

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Abstract

Motion of the upper limbs is often coupled to that of the lower limbs in human bipedal locomotion. It is unclear, however, whether the functional coupling between upper and lower limbs is bi-directional, i.e. whether arm movements can affect the lumbosacral locomotor circuitry. Here we tested the effects of voluntary rhythmic arm movements on the lower limbs. Participants lay horizontally on their side with each leg suspended in an unloading exoskeleton. They moved their arms on an overhead treadmill as if they walked on their hands. Hand-walking in the antero-posterior direction resulted in significant locomotor-like movements of the legs in 58% of the participants. We further investigated quantitatively the responses in a subset of the responsive subjects. We found that the electromyographic (EMG) activity of proximal leg muscles was modulated over each cycle with a timing similar to that of normal locomotion. The frequency of kinematic and EMG oscillations in the legs typically differed from that of arm oscillations. The effect of hand-walking was direction specific since medio-lateral arm movements did not evoke appreciably leg air-stepping. Using externally imposed trunk movements and biomechanical modelling, we ruled out that the leg movements associated with hand-walking were mainly due to the mechanical transmission of trunk oscillations. EMG activity in hamstring muscles associated with hand-walking often continued when the leg movements were transiently blocked by the experimenter or following the termination of arm movements. The present results reinforce the idea that there exists a functional neural coupling between arm and legs.

Highlights

Humans swing the arms in an automatic, stereotypical way during locomotion by pairing upper and lower limb movements with integer ratio frequencies, as do animals during quadrupedal locomotion [1,2,3,4]
Participants In a first series of experiments, we screened 33 healthy volunteers naıve to the purpose of the experiments for the presence of leg responses. Nine of these subjects, in whom prominent leg movements could be elicited by arm movements and who were able to return to the laboratory to participate in additional sessions, were selected for detailed kinematic and EMG recordings in a second series of experiments
To reduce the attention level paid to the locomotor task, participants were always asked to carry out mental arithmetic throughout a trial

Summary

Introduction

Humans swing the arms in an automatic, stereotypical way during locomotion by pairing upper and lower limb movements with integer ratio frequencies, as do animals during quadrupedal locomotion [1,2,3,4]. These arm movements are characteristic of walking, running, crawling, swimming, climbing and other gaits, but they are not obligatory (as when we walk with crossed arms). Inter-limb coordination may reflect supraspinal control; hindlimb-related neurons in cat motor cortex respond to changes in forelimb movements during locomotion [20]

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