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,1McGeer T. Passive dynamic walking.Int. J. Robot Res. 1990; 9: 62-82Crossref Scopus (2509) Google Scholar,2McHenry M.J. Anderson P.S.L. Van Wassenbergh S. Matthews D.G. Summers A.P. Patek S.N. The comparative hydrodynamics of rapid rotation by predatory appendages.J. Exp. Biol. 2016; 219: 3399-3411Crossref PubMed Scopus (23) Google Scholar whereas intrinsic forces are generated by active muscle contraction or passive musculoskeletal elements.3Burrows M. Shaw S.R. Sutton G.P. Resilin and chitinous cuticle form a composite structure for energy storage in jumping by froghopper insects.BMC Biol. 2008; 6: 41Crossref PubMed Scopus (117) Google Scholar,4Ache J.M. Matheson T. Passive joint forces are tuned to limb use in insects and drive movements without motor activity.Curr. Biol. 2013; 23: 1418-1426Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar For lightweight appendages, such as insect limbs, movements depend more upon intrinsic than extrinsic forces.5Hooper S.L. Guschlbauer C. Blümel M. Rosenbaum P. Gruhn M. Akay T. Büschges A. Neural control of unloaded leg posture and of leg swing in stick insect, cockroach, and mouse differs from that in larger animals.J. Neurosci. 2009; 29: 4109-4119Crossref PubMed Scopus (70) Google Scholar,6Charles S.K. Hogan N. Stiffness, not inertial coupling, determines path curvature of wrist motions.J. Neurophysiol. 2012; 107: 1230-1240Crossref PubMed Scopus (27) Google Scholar Indeed, passive movements of insect limbs can be large and oppose or aid joint flexion, extension, or both.4Ache J.M. Matheson T. Passive joint forces are tuned to limb use in insects and drive movements without motor activity.Curr. Biol. 2013; 23: 1418-1426Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar Yet, how passive properties contribute to insects’ goal-directed limb movements, such as targeted reaching and searching,7Niven J.E. Buckingham C.J. Lumley S. Cuttle M.F. Laughlin S.B. Visual targeting of forelimbs in ladder-walking locusts.Curr. Biol. 2010; 20: 86-91Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar,8Niven J.E. Ott S.R. Rogers S.M. Visually targeted reaching in horse-head grasshoppers.Proc. Biol. Sci. 2012; 279: 3697-3705PubMed Google Scholar,9Pick S. Strauss R. Goal-driven behavioral adaptations in gap-climbing drosophila.Curr. Biol. 2005; 15: 1473-1478Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar,10Blaesing B. Cruse H. Stick insect locomotion in a complex environment: Climbing over large gaps.J. Exp. Biol. 2004; 207: 1273-1286Crossref PubMed Scopus (91) Google Scholar 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.