Abstract
Like other animals, lampreys have a central pattern generator (CPG) circuit that activates muscles for locomotion and also adjusts the activity to respond to sensory inputs from the environment. Such a feedback system is crucial for responding appropriately to unexpected perturbations, but it is also active during normal unperturbed steady swimming and influences the baseline swimming pattern. In this study, we investigate different functional forms of body curvature-based sensory feedback and evaluate their effects on steady swimming energetics and kinematics, since little is known experimentally about the functional form of curvature feedback. The distributed CPG is modeled as chains of coupled oscillators. Pairs of phase oscillators represent the left and right sides of segments along the lamprey body. These activate muscles that flex the body and move the lamprey through a fluid environment, which is simulated using a full Navier-Stokes model. The emergent curvature of the body then serves as an input to the CPG oscillators, closing the loop. We consider two forms of feedback, each consistent with experimental results on lamprey proprioceptive sensory receptors. The first, referred to as directional feedback, excites or inhibits the oscillators on the same side, depending on the sign of a chosen gain parameter, and has the opposite effect on oscillators on the opposite side. We find that directional feedback does not affect beat frequency, but does change the duration of muscle activity. The second feedback model, referred to as magnitude feedback, provides a symmetric excitatory or inhibitory effect to oscillators on both sides. This model tends to increase beat frequency and reduces the energetic cost to the lamprey when the gain is high and positive. With both types of feedback, the body curvature has a similar magnitude. Thus, these results indicate that the same magnitude of curvature-based feedback on the CPG with different functional forms can cause distinct differences in swimming performance.
Highlights
To move effectively, all animals must activate their muscles to move their bodies
The muscles in the model are activated by a central pattern generator (CPG), which is approximated as a set of phase oscillators that receive input from each other and from the body’s curvature through a feedback function
The initial conditions chosen for the phase oscillators did not affect the steady state swimming results, as long as the chains were not initialized with exactly the same phases
Summary
All animals must activate their muscles to move their bodies. In nearly every animal studied, this pattern of muscle activation is produced by a relatively small neural circuit called a central pattern generator (CPG) [1, 2], which is influenced by the mechanics of their bodies and the physical world around them. The primary proprioceptors in lampreys are mechanosensory cells, called edge cells, and are located on the spinal cord [5], in contrast to the proprioceptive muscle spindles and Golgi tendon organs of mammals, which are located in the periphery [6]. These edge cells synapse onto several different classes of ventral horn interneurons that make up the CPG [7]. Muscle spindles have similar effects on the CPG [12]
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