Chen Li

To traverse complex terrain, animals often transition between locomotor modes. It is well known that locomotor transitions can be induced by switching in neural control circuits or driven by a need to minimize metabolic energetic cost. Recent work revealed that locomotor transitions in complex 3D terrain cluttered with large obstacles can emerge from physical interaction with the environment controlled by the nervous system. For example, to traverse cluttered, stiff grass-like beams, the discoid cockroach often transitions from using a strenuous pitch mode pushing across the beams to using a less strenuous roll mode rolling into and through the gaps. This transition can save mechanical energetic cost substantially (∼100–101 mJ) but requires overcoming a potential energy barrier (∼10−3–10−2 mJ). Previous robotic physical modeling demonstrated that kinetic energy fluctuation of body oscillation from self-propulsion can help overcome the barrier and facilitate this transition. However, the animal was observed to transition even when the barrier still exceeded kinetic energy fluctuation. Here, we further studied whether and how the cockroach makes active adjustments to facilitate this transition to traverse cluttered beams. The animal repeatedly flexed its head and abdomen, reduced hindleg sprawl, and depressed one hindleg and elevated the other during the pitch-to-roll transition, adjustments which were absent when running on a flat ground. Using a refined potential energy landscape with additional degrees of freedom to model these adjustments, we found that head flexion did not substantially reduce the transition barrier (by ∼10−3 mJ), whereas leg sprawl reduction did so dramatically (by ∼10−2 mJ). We speculate that head flexion is for sensing the terrain to guide the transition via sensory feedback control.