Multi-timescale motor circuit dynamics underlie adaptive and efficient exploratory behavior

Motor systems must balance stability and flexibility to enable efficient and adaptive movements, yet the circuit-level mechanisms generating their intrinsic dynamics remain poorly understood. Here, we investigate the head exploratory behavior of Caenorhabditis elegans, a minimal system capable of intricate motor patterns. Using variational mode decomposition, we identified two distinct motor dynamics: slow rhythmic bends propagating along the body and fast, phase-specific head casts influencing directional bias. Combinatorial ablations of three classes of cholinergic motor neurons, in conjunction with dynamical systems analysis, revealed their distinct and overlapping roles: RMD contributes to head casts, SMD sustains bending states, and SMB and SMD enable slow rhythmic bending and head-body coupling. Collectively, these neurons form a major rhythm generator that sustains undulatory forward locomotion. We propose a model where dual-proprioceptive feedback operates across multiple timescales, with slow feedback coordinating rhythmic bending and fast feedback shaping head casts to optimize roaming efficiency. Our findings highlight how complex, structured dynamics emerge from highly interactive low-level circuits.