The velocity-curvature power law in Drosophila larval locomotion

Abstract

We report the discovery that the locomotor trajectories generated by crawling fruit fly larvae follow the same power law relationship between speed and curvature previously found in the human motor control of hand-drawing, walking, eye movements and speech. Using high resolution behavioral tracking of individual flies in different sensory environments, we tested the power law by making maggots trace different trajectory types in naturalistic conditions, from reaching-like movements to scribbles. In all these conditions, we found that the law holds, and also that the exponent of the larval scaling law approaches 3/4, rather than the usual 2/3 exponent found in almost all human situations. This is consistent with recent findings on humans drawing ellipses on water, where dynamic effects related to medium viscosity have been shown to increase the exponent that would emerge from purely kinematic-geometric constraints. To our knowledge, the speed-curvature power law has only been studied in human and non-human primates, our work then being the first demonstration of the speed-curvature scaling principle in other species. As there are still different competing hypotheses for the origin of such law in humans (one invoking complex cortical computations in primates; another postulating its emergence from the coupling of viscoelastic muscle properties with simple central pattern generation) our findings in the larva demonstrate that the law is possible in an animal with a nervous system orders of magnitude simpler than that of humans, thus supporting the latter view. Given that our discovery is in Drosophila (amenable to precise genetic manipulations, electron microscopy reconstruction of neural circuits, imaging in behaving animals, electrophysiology, and other techniques) this opens great potential for uncovering the mechanistic implementation of the velocity-curvature power law. Such scaling laws might exist because natural selection favors processes that remain behaviorally efficient across a wide range of contexts in distantly related species. Our work is an effort to search for shared principles of animal behavior across phyla.