Emergence of the advancing neuromechanical phase in a resistive force dominated medium

Undulatory locomotion, a gait in which thrust is produced in the opposite direction of a traveling wave of body bending, is a common mode of propulsion used by animals in fluids, on land, and even within sand. As such, it has been an excellent system for discovery of neuromechanical principles of movement. In nearly all animals studied, the wave of muscle activation progresses faster than the wave of body bending, leading to an advancing phase of activation relative to the curvature toward the tail. This is referred to as "neuromechanical phase lags" (NPL). Several multiparameter neuromechanical models have reproduced this phenomenon, but due to model complexity, the origin of the NPL has proved difficult to identify. Here, we use perhaps the simplest model of undulatory swimming to predict the NPL accurately during sand-swimming by the sandfish lizard, with no fitting parameters. The sinusoidal wave used in sandfish locomotion, the friction-dominated and noninertial granular resistive force environment, and the simplicity of the model allow detailed analysis, and reveal the fundamental mechanism responsible for the phenomenon: the combination of synchronized torques from distant points on the body and local traveling torques. This general mechanism should help explain the NPL in organisms in other environments; we therefore propose that sand-swimming could be an excellent system with which to generate and test other neuromechanical models of movement quantitatively. Such a system can also provide guidance for the design and control of robotic undulatory locomotors in complex environments.