Capturing the continuous complexity of natural behavior

While animal behavior is often quantified through discrete motifs, this is only an approximation to fundamentally continuous dynamics and ignores important variability within each motif. Here, we develop a behavioral phase space in which the instantaneous state is smoothly unfolded as a combination of postures and their short-time dynamics. We apply this approach to C. elegans and show that the dynamics lie on a 6D space, which is globally composed of three sets of cyclic trajectories that form the animal’s basic behavioral motifs: forward, backward and turning locomotion. In contrast to global stereotypy, variability is evident by the presence of locally-unstable dynamics for each set of cycles. Across the full phase space we show that the Lyapunov spectrum is symmetric with positive, chaotic exponents driving variability balanced by negative, dissipative exponents driving stereotypy. The symmetry of the spectrum holds for different environments and for human walking, suggesting a general condition of motor control. Finally, we use the reconstructed phase space to analyze the complexity of the dynamics along the worm’s body and find evidence for multiple, spatially-separate oscillators driving C. elegans locomotion.