Perturbation of leg protraction causes context-dependent modulation of inter-leg coordination, but not of avoidance reflexes

Abstract

All animals capable of legged locomotion execute fast, adaptive compensatory movements in response to perturbation of a step cycle. In terms of motor control, such adaptive behaviour typically involves changes in the kinematics of the perturbed limb as well as changes in coordination between legs. Moreover, the unpredictable variety of real life situations implies that compensatory responses should be sensitive to the behavioural context of the animal. We have investigated the extent to which the compensatory response of a walking stick insect (Carausius morosus) adapts in parallel to strong context-dependent adaptation of step kinematics and inter-leg coordination. The behavioural contexts we chose were straight walking and visually induced curve walking, for both of which the steady state limb kinematics and inter-leg coupling strengths were known. In case of curve walking, we further distinguished contexts according to whether the inner or the outer leg was perturbed. The three contexts differed strongly with respect to the set of joint actions before perturbation. Upon mechanical perturbation of front leg protraction, we studied context-dependent differences in a local avoidance reflex of the perturbed leg, as well as in coordination mechanisms that couple the step cycles of the perturbed leg to its unperturbed neighbours. In all three walking contexts, obstacle contact caused an avoidance movement of the front leg that deviated from the unperturbed swing trajectory. Swing duration was increased while step distance was decreased; however, both effects vanished in the subsequent unperturbed step. The prevailing immediate reaction of the three leg joints were retraction of the coxa (>76%), levation of the femur (>80%), and flexion of the tibia (>80%), regardless of the behavioural context and, therefore, joint action prior to perturbation. Moreover, activation of each one of these joint actions was shown to be independent of the other two. Thus, local avoidance reflexes are not modulated by the descending visual information that causes transition from straight to curve walking, but are composed of context-independent joint actions. Perturbation of the front leg also caused significant shifts of the touch-down position of the perturbed leg and of its unperturbed neighbours. If the inner front leg was perturbed, this shift could persist until the subsequent step. Perturbation affected both the spatial location and the timing of touch-down and lift-off transitions in unperturbed neighbouring legs. These effects on inter-leg coordination were context-dependent. For example, time delay to lift-off of the contralateral neighbour was shortened in inner and straight walking legs, but not in outer legs. Finally, a targeting mechanism that determines foot placement in stick insects was shown to be affected by perturbation in a context-dependent manner. We conclude that the immediate compensatory response of the perturbed leg is not adapted to the behavioural context in spite of strongly differing step kinematics, whereas the compensatory effect on inter-limb coupling is context-dependent.