Instantaneous kinematic phase reflects neuromechanical response to lateral perturbations of running cockroaches

Shai Revzen, Samuel A. Burden, Talia Y. Moore, Jean-Michel Mongeau, Robert J. Full

Instantaneous kinematic phase calculation allows the development of reduced-order oscillator models useful in generating hypotheses of neuromechanical control. When perturbed, changes in instantaneous kinematic phase and frequency of rhythmic movements can provide details of movement and evidence for neural feedback to a system-level neural oscillator with a time resolution not possible with traditional approaches. We elicited an escape response in cockroaches (Blaberus discoidalis) that ran onto a movable cart accelerated laterally with respect to the animals' motion causing a perturbation. The specific impulse imposed on animals (0.50 [Formula: see text] 0.04 m s[Formula: see text]; mean, SD) was nearly twice their forward speed (0.25 [Formula: see text] 0.06 m s[Formula: see text]. Instantaneous residual phase computed from kinematic phase remained constant for 110 ms after the onset of perturbation, but then decreased representing a decrease in stride frequency. Results from direct muscle action potential recordings supported kinematic phase results in showing that recovery begins with self-stabilizing mechanical feedback followed by neural feedback to an abstracted neural oscillator or central pattern generator. Trials fell into two classes of forward velocity changes, while exhibiting statistically indistinguishable frequency changes. Animals pulled away from the side with front and hind legs of the tripod in stance recovered heading within 300 ms, whereas animals that only had a middle leg of the tripod resisting the pull did not recover within this period. Animals with eight or more legs might be more robust to lateral perturbations than hexapods.