Corticomuscular coherence revealed during treadmill walking: further evidence of supraspinal control in human locomotion

摘要

It is generally assumed that precision tasks, such as carving or painting, require a lot of attention and cortical control, whereas walking in the street may be considered as an automatic movement based on reflexes governed at the spinal level. A very recent study in The Journal of Physiology by Petersen et al. (2012) demonstrates that the motor cortex is particularly active during specific phases of the gait cycle, before the foot comes in contact with the ground. This is a new piece added to the gigantic puzzle of the neural control of human locomotion. Accumulating evidence suggests that human locomotion is based on a very complex hierarchical system that includes several control networks located at both spinal and supraspinal levels. The spinal central pattern generator network consists of coupled antagonist oscillators specifically dedicated to extensor or flexor muscles acting at the different joints. Their mechanism allows the generation of simple and co-ordinated rhythmic movements, such as those involved in steady walking. Numerous experiments with spinal cats (i.e. cats with complete transection of the spinal cord) have demonstrated the presence of such central pattern generators in lower mammals, and a similar conclusion has been reached for primates. Regarding humans, the evidence is only indirect, as reported by Yang & Gorassini (2006). Although the existence (and primary function) of a central pattern generator system in humans has become broadly accepted, many findings indicate that the cortex also plays an important role in human walking (Yang & Gorassini, 2006). Indeed, when lesions occur in the supraspinal region of the CNS, recovery of walking is extremely difficult and generally incomplete. This means that intact supraspinal centres are necessary for functional walking in humans. Also, studies of direct transcranial magnetic stimulation of neurons in the motor cortex have shown that the motor cortex is likely to play a role in activating the dorsiflexors and plantarflexors during walking in humans (Petersen et al. 2001). Additionally, as summarized by Presacco et al. (2011) and references therein, significant changes in motor and cognitive demands (i.e. spatial attention) have been observed in the context of bipedal walking in unknown or cluttered dynamic environments. Functional neuroimaging studies have shown that the primary motor cortex is recruited during rhythmic foot or leg movements. Functional near-infrared spectroscopy has also allowed the detection of involvement of the frontal, premotor and supplementary motor areas during walking. Finally, electrophysiological studies have provided arguments in favour of the possible cortical origin of the intramuscular and intermuscular EMG synchronization (coherence) observed in lower limbs during walking. In this context, the work by Petersen et al. (2012) was aimed at investigating the coupling between EEG and EMG signals from leg muscles during treadmill walking. The authors report significant coherence between EEG signals recorded over the leg motor area (Cz electrode) and EMG from the tibialis anterior muscle in the 24–40 Hz frequency band before the heel strike, during the swing phase of the gait cycle. This result indicates that rhythmic cortical activity in this particular frequency band is transmitted to the lower limb muscles during walking. This work thus proves and confirms that the motor cortex contributes directly to the muscle activity involved in human locomotion. The significant coherence values found for normal walking speeds (3.5–4 km h−1) are located between −700 and −200 ms (with a peak between −450 and −350 ms) before the heel strike. Significant coupling from 8 to 12 Hz, with distinct peaks in early, mid- and late swing, was also observed. The same analysis was done with recordings made during slow walking (1 km h−1), and analogous results were found, except that the 24–40 Hz coherence was more pronounced from −500 to −400 ms prior to h