Braking slows passive flexion during goal-directed movements of a small limb

Abstract

The movements of animal appendages are determined by extrinsic and intrinsic forces. Extrinsic forces include gravity or friction,1,2 whereas intrinsic forces are generated by active muscle contraction or passive musculoskeletal elements.3,4 For lightweight appendages, such as insect limbs, movements depend more upon intrinsic than extrinsic forces.5,6 Indeed, passive movements of insect limbs can be large and oppose or aid joint flexion, extension, or both.4 Yet, how passive properties contribute to insects' goal-directed limb movements, such as targeted reaching and searching,7-10 remains unclear. Here, we show that mantids make targeted reaches and searches to objects by using their raptorial forelimbs, employing braking to slow passive flexion of the femoro-tibial (FTi) joint. In most reaches, tibial flexion ensures the forelimb contacts the object. Such tibial flexion is particularly clear when the forelimb misses the object and continues on a downward trajectory or during directed searching movements. We characterize the passive properties of the FTi joint by combining passive movements of excised limbs with apodeme ablations and muscle stimulation. These experiments show that passive properties of the flexor tibiae muscle-apodeme complex are the primary structural element producing tibial flexion in excised limbs. During reaching and searching, however, tibial flexion is slower and smaller than predicted. This is due to braking, which opposes passive flexion, thereby reducing the magnitude and velocity of tibial flexion. Braking retarding passive movements is a novel behaviorally relevant control strategy for the goal-directed movements of lightweight limbs, such as those of insects.