The Metastability of the Double-Tripod Gait in Locust Locomotion

Insect locomotion represents a fundamental example of neuronal oscillating circuits generating different motor patterns or gaits by controlling their phase coordination. Walking gaits are assumed to represent stable states of the system, often modeled as coupled oscillators. This view is challenged, however, by recent experimental observations, in which in vitro locust preparations consistently converged to synchronous rhythms (all legs oscillating as one), a locomotive pattern never seen in vivo. To reconcile this inconsistency, we developed a modeling framework to capture the trade-off between the two competing mechanisms: the endogenous neuronal circuitry, expressed in vitro, and the feedback mechanisms from sensory and descending inputs, active only in vivo. We show that the ubiquitously observed double-tripod walking gait emerges precisely from this balance. The outcome is a short-lived meta-stable double-tripod gait, which transitions and alternates with stable idling, thus recovering the observed intermittent bouts of locomotion, typical of many insects' locomotion behavior.