Breaking Symmetry in Walking: Drosophila Recruits Task- and Leg-Specific Motor Modules for Curve Walking
Walking animals must continuously reorient to navigate their environment, yet how leg kinematics are reconfigured to produce directional changes of varying magnitude remains poorly understood. Here, we used high-resolution leg tracking to characterize steering behavior in freely walking Drosophila. We focus our analysis on two major strategies, arcs and turns. Although arc and turn trajectories are statistically separable, several parameters suggest an underlying spatial continuum spanning both behavioral categories, involving a change in the steering mechanism rather than a discontinuity in the kinematic space. Arcs, representing shallow curves, and were generated primarily through: (1) graded shifts in the posterior extreme position (PEPs) of the front and inside middle legs, and bilateral asymmetries in stance amplitude, lengthening on the outside (2) and shortening on the inside (3) while step timing and ipsilateral coordination remained at straight-walking baseline. Turns, in contrast, were associated with higher steering demands and relied on: (4) progressive displacement of the anterior extreme positions (AEPs) in front and middle legs, (5) extreme reduction of inside middle and hind leg amplitudes to anchor the turning pivot, (6) skipped steps of inside middle and hind legs, (7) lateral steps of inside middle legs, and (8) spontaneous appearance of synchronized backward-stepping in particular legs beyond a critical turning threshold. Finally, a common kinematic configuration emerges at maximal turning demand. These results suggest a hierarchical, bipartite organization of steering: PEP- and AEP-driven mechanisms operating across moderate and severe trajectory curvatures, and a shared saturated motor state at the behavioral extreme that links descending steering commands to segment-specific leg kinematics in a freely walking insect