Motor module activation sequence and topography in the spinal cord during air-stepping in human: Insights into the traveling wave in spinal locomotor circuits.

Coordinated locomotor muscle activity is generated by the spinal central pattern generators (CPGs), which are modulated by peripheral and supraspinal inputs. The CPGs would consist of multiple motor modules generating basic muscle activity, which are distributed rostrocaudally along the spinal cord. To activate the motor modules in proper sequence, rostrocaudally traveling waves of activation in the spinal cord are important mechanisms in the CPGs. The traveling waves of activation have been observed in nonhuman vertebrates. However, they have not yet been confirmed during human locomotion. Although, rostrocaudal wave-like activations in the spinal cord were observed during walking in humans in a previous study, the propagation shifted rostrally toward the upper lumbar segments at foot contact. Here, using an air stepping task to remove the foot-contact interactions, we examined whether the traveling wave mechanism exists in the human spinal circuits based on the activation sequence of motor modules and their topography. We measured electromyographic activity of lower leg muscles during the air-stepping task. Then, we extracted motor modules (i.e., basic patterns of sets of muscle activations: muscle synergies) from the measured muscle activities using nonnegative matrix factorization method. Next, we reconstructed motoneuron (MN) activity from each module activity based on myotomal charts. We identified four types of motor modules from muscle activities during the air-stepping task. Each motor module represented different sets of synergistic muscle activations. MN clusters innervating each motor module were sequentially activated from the rostral to caudal region in the spinal cord, from the initial flexion to the last extension phase during air-stepping. The rostrocaudally sequential activation of MN clusters suggests the possibility that rostrocaudally traveling waves exist in human locomotor spinal circuits. The present results advance the understanding of human locomotor control mechanisms, and provide important insights into the evolution of locomotor networks in vertebrates.