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

Motor systems must balance flexibility and structure to enable efficient and adaptive movements. Traditional hierarchical descending models struggle to explain the intrinsic dynamism in natural behaviors. 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 types 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, SMB and SMD enable slow rhythmic bending and head-body coupling. Collectively, these neurons form a central pattern generator (CPG) driving forward locomotion. In addition, RMD subgroups displayed unique calcium dynamics correlated with rapid head movements and slow transitions between behavior states. We propose that dual-proprioceptive feedback underlies these multi-timescale dynamics, with slow feedback coordinating rhythmic bending and fast feedback shaping head casts, thereby optimizing roaming efficiency. These findings highlight how intrinsic dynamics and structured composition emerge from highly interactive low-level circuits.