Neuromuscular control of free-flight yaw turns in the hawkmothManduca sexta

Abstract

The biomechanical properties of an animal's locomotor structures profoundly influence the relationship between neuromuscular inputs and body movements. In particular, passive stability properties are of interest as they may offer a non-neural mechanism for simplifying control of locomotion. Here, we hypothesized that a passive stability property of animal flight, flapping counter-torque (FCT), allows hawkmoths to control planar yaw turns in a damping-dominated framework that makes rotational velocity directly proportional to neuromuscular activity. This contrasts with a more familiar inertia-dominated framework where acceleration is proportional to force and neuromuscular activity. To test our hypothesis, we collected flight muscle activation timing, yaw velocity and acceleration data from freely flying hawkmoths engaged in planar yaw turns. Statistical models built from these data then allowed us to infer the degree to which the moths inhabit either damping- or inertia-dominated control domains. Contrary to our hypothesis, a combined model corresponding to inertia-dominated control of yaw but including substantial damping effects best linked the neuromuscular and kinematic data. This result shows the importance of including passive stability properties in neuromechanical models of flight control and reveals possible trade-offs between manoeuvrability and stability derived from damping.