The kinematics and neural control of high-speed kicking movements in the locust.

Abstract

The tibiae of locust hind legs can be extended fully in a kick in 3 ms with peak angular velocities of at least 80 degrees ms(-1). If the mass of the distal part of the leg is halved, then the extension is complete in less than 1 ms with angular velocities of more than 200 degrees ms(-1). The high velocities and the associated power are generated by a preceding storage of energy and its sudden release produced by a specific motor pattern and specialisations of the femoro-tibial joints. To understand the dynamics of these rapid movements and the interrelations between joint mechanics and the motor pattern, kicks were analysed with high-speed video images coupled to simultaneous intracellular recordings from identified leg motor neurones. The first movement is a full tibial flexion followed by co-contraction of the extensor and flexor tibiae muscles for 0.3-1 s, during which the distal end of the femur is flattened dorso-ventrally and expanded laterally. The two semi-lunar processes on the distal femur are bent when the fast extensor tibiae motor neurone spikes so that their tips move ventrally by up to 0.6 mm. The inward projections of these processes into the femur form the proximal part of the hinge joint with the tibia, so that the pivot of the joint also changes and the tibia therefore moves proximally and ventrally, widening the gap between it and the femur. Extension of the tibia begins on average 34 ms after the flexor motor neurones are inhibited at the end of the co-contraction phase. The tibia then begins to extend slowly, reaching peak velocities only when it has extended by 60-70 degrees. The semi-lunar processes do not start to unfurl until the tibia has extended by 55 degrees, so they cannot provide the initial energy for extension. An audible click is produced when the semi-lunar processes unfurl. The peak velocity of tibial extension is correlated with the amount of bending of the semi-lunar processes and with the number of fast extensor motor spikes, but the same amount of semi-lunar bending can be produced by both short and long co-contractions. When the tibia reaches full extension, inertial forces may cause it to bend by as much as 33 degrees at a plane of weakness in the proximal tibia, thus allowing further extension of the distal end.