Strong environmental forces induce a loss of wave coherence in C. elegans*

Undulation is a locomotor strategy employed by a large group of organisms that vary dramatically in scale and natural habitat.  This form of locomotion generally involves the coherent propagation of waves of body curvature along the body of the organism, producing thrust. Coordination of undulatory waves is thought to be regulated by a quasi-redundant set of control mechanisms, 1) feedforward commands 2) sensory feedback and 3) passive mechanical processes that arise from physical body-environment interactions. The presence of strong environmental perturbations, such as obstacles or highly resistive media (e.g. packed soil), can disrupt wave coherence, producing more complex body kinematics (e.g. multi-frequency undulation, wave interference, quasi-periodicity, and aperiodic states). We describe the origin of these behaviors in the mm-scale nematode C. elegans moving in viscoelastic gels (bulk modulus ~1-50nN/ μm²) by isolating environmental effects on the various control systems. Exploiting its suite of available genetic tools, we performed functional imaging of muscle activity and also compared the loss of wave coherence in mutants with defective mechanosensory feedback mechanisms (local proprioception and global touch sensation) to wild-type animals. Our results suggest that environmental perturbations affect multiple control systems to induce incoherent undulatory dynamics under increasing environmental forces, producing the observed behavioral complexity.