Proprioceptors monitoring forces in a locust hind leg during kicking form negative feedback loops with flexor tibiae motor neurons.

Abstract

In preparation for jumping and kicking, a locust slowly generates large forces in the femoral muscles of its hind legs and stores them in elastic distortions of the tendons and femoral cuticle. At the femoro-tibial joints, the semi-lunar processes are bent, the cuticle of the dorsal distal femur is crumpled, and the femur is expanded in a mediolateral direction. We have analysed whether these distortions are monitored by sense organs and whether the information they provide is used to limit the forces generated and thus prevent structural damage to the joint. The two sensory neurons comprising the lump receptor lie in a groove in the ventral part of the distal femur. The sensory neurons spike if force is applied to the flexor tendon when the joint is fully flexed, but not when it is extended. They also spike as the tendon of the flexor muscle slides into the ventral femoral groove when the tibia is fully flexed during the co-contraction phase of kicking. Their spike frequency correlates with the extent of bending of a semi-lunar process that provides a quantifiable measure of the joint distortions. If the tibia is not fully flexed, however, then muscle contractions still cause distortions of the joint but these are not signalled by sensory spikes from the lump receptor. The lump receptor, therefore, does not respond primarily to the joint distortions but to the movements or force in the flexor tendon. Contractions of the flexor tibiae muscle caused by spikes in individual flexor motor neurons can evoke spikes in sensory neurons from the lump receptor when the joint is fully flexed. In turn, the sensory neurons cause a hyperpolarisation in particular flexor motor neurons in a polysynaptic negative feedback loop. The lump receptor could, therefore, regulate the output of the flexor motor neurons and, thus, limit the amount of force generated during co-contraction. It may also contribute to the inhibition of the flexors at the end of co-contraction that allows rapid kicking movements to occur.