Emergent Simplicity and Multiscale Mechanisms of Agile Animal Movement
The ability to move is a trait of all animals. Yet how do animals, including ourselves, get around in this complex and uncertain world with an ease and agility we find hard to recreate in engineered systems? Using an organismal physics approach my group explores the physical and physiological mechanisms that enable agile movement in living systems. I will discuss studies at three scales in animal movement. We first examine flight maneuvers as emergent dynamics from the underlying complex physiological systems. Using robophysical models of flowers, we probed how maneuverable, hovering hawk moths to adjust to light levels that vary by 7 orders of magnitude from early afternoon to late dusk. Using simple one-parameter models from control theory we discover the brain slows its visual processing to accomplish temporal summation in dim light – like increasing the exposure time on a camera. Perhaps more surprisingly the resulting dynamics are empirically linear, invariant under experimental scaling and superposition. This allows us to predict behavior to novel stimulus combinations. We next investigate the neural basis of these behaviors by recording a comprehensive motor program – all the electrical signals that the moth’s brain sends to it wings. The brains of small flapping insects are still complex, with 105-106 neurons, but we find that they control wingstroke dynamics with as few as 101 motor units that mostly utilize precise timing to inform torque. Finally we explored how muscle’s macroscopic properties during locomotion are shaped by its unusual multiscale structure. High-speed x-ray diffraction through living muscles shows that muscle is active crystalline matter – the regular arrangement of actin and myosin filaments produces a lattice that dynamically changes spacing as a muscle contracts. As a result, muscle has a time-varying poisson ratio including an auxetic regime and these dynamics result in flow that assists the convective delivery of molecules. Moreover a single nanometer difference in muscle lattice spacing can account for how one muscle acts like a motor while another acts like a brake. We cannot yet emulate the motility seen in nature, nor derive behavior, but the emergent dynamics of animal locomotion is an exciting opportunity.