Locomotor resilience through load-dependent modulation of muscle co-contraction

Terrestrial locomotor behavior in variable environments requires resilience to sudden changes in substrate properties. For example, walking animals can adjust to substantial changes in slope and corresponding changes in load distribution among legs. In insects, slope-dependent adjustments have mainly been examined under steady-state conditions, whereas the transition dynamics have been largely neglected. In a previous study, we showed that steady-state adjustments of stick insects to ±45 deg slopes involve substantial changes in joint torques and muscle activity with only minor changes in leg kinematics. Here, we took a close look at the time course of these adjustments as stick insects compensate for various kinds of disturbances to load distribution. In particular, we tested whether the transition from one steady state to another involves distinct transition steps or follows a graded process. To resolve this, we combined simultaneous recordings of whole-body kinematics and hindleg muscle activity to elucidate how freely walking Carausius morosus negotiated a step-change in substrate slope. Step-by-step adjustments revealed that muscle activity changed in a graded manner as a function of body pitch relative to gravity. We further show analogous transient adjustment of muscle activity in response to destabilizing lift-off events of neighboring legs and the disappearance of antagonist co-activation during crawling episodes. Given these three examples of load-dependent regulation of antagonist muscle co-contraction, we conclude that stick insects respond to both transient and sustained changes in load distribution by regulating joint stiffness rather than through distinct transition steps.