Motor unit mechanisms of speed control in mouse locomotion

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Abstract

During locomotion, the coordinated activity of dozens of muscles shapes the kinematic features of each stride, including systematic changes in limb movement across walking speed. Motor units, each of which consists of a single motor neuron and the muscle fibers it innervates, contribute to the total activation of each muscle through their recruitment and firing rate when active. However, it remains unknown how the nervous system controls locomotor speed by changing the firing of individual motor units. To address this, we combined quantitative behavioral analysis of mouse locomotion with single motor unit recordings from the lateral and long heads of the triceps brachii, which drive monoarticular extension of the elbow and biarticular movements of the elbow and shoulder, respectively. In contrast to prior studies employing bulk EMG to examine muscle activity, our recordings revealed the diversity of spike patterning across motor units as well as systematic differences in motor unit activity across muscles and locomotor speeds. First, motor unit activity differed significantly across the lateral and long heads, suggesting differential control of these two closely apposed elbow extensor muscles. Second, we found that individual units were recruited probabilistically during only a subset of strides, showing that bulk EMG signals consistently present in every stride in fact reflect stochastically varying subsets of individual motor units. Finally, although recruitment probability and firing rate both increased at faster walking speeds, increases in recruitment were proportionally larger than rate changes, and recruitment of individual units accompanied changes in limb kinematics. Together, these results reveal how the firing of individual motor units varies systematically across muscles and walking speeds to produce flexible locomotor behavior.

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