Mechanisms underlying rhythmic locomotion: interactions between activation, tension and body curvature waves

Abstract

Undulatory animal locomotion arises from three closely related propagating waves that sweep rostrocaudally along the body: activation of segmental muscles by motoneurons (MNs), strain of the body wall, and muscle tension induced by activation and strain. Neuromechanical models that predict the relative propagation speeds of neural/muscle activation, muscle tension and body curvature can reveal crucial underlying control features of the central nervous system and the power-generating mechanisms of the muscle. We provide an analytical explanation of the relative speeds of these three waves based on a model of neuromuscular activation and a model of the body-fluid interactions for leech anguilliform-like swimming. First, we deduced the motoneuron spike frequencies that activate the muscle and the resulting muscle tension during swimming in intact leeches from muscle bending moments. Muscle bending moments were derived from our video-recorded kinematic motion data by our body-fluid interaction model. The phase relationships of neural activation and muscle tension in the strain cycle were then calculated. Our study predicts that the MN activation and body curvature waves have roughly the same speed (the ratio of curvature to MN activation speed ≈0.84), whereas the tension wave travels about twice as fast. The high speed of the tension wave resulting from slow MN activation is explained by the multiplicative effects of MN activation and muscle strain on tension development. That is, the product of two slower waves (activation and strain) with appropriate amplitude, bias and phase can generate a tension wave with twice the propagation speed of the factors. Our study predicts that (1) the bending moment required for swimming is achieved by minimal MN spike frequency, rather than by minimal muscle tension; (2) MN activity is greater in the mid-body than in the head and tail regions; (3) inhibitory MNs not only accelerate the muscle relaxation but also reduce the intrinsic tonus tension during one sector of the swim cycle; and (4) movements of the caudal end are passive during swimming. These predictions await verification or rejection through further experiments on swimming animals.