An elaborate tension receptor system highlights sensory complexity in the hind leg of the locust

The tibia of each leg of the locust is moved by two antagonistic muscles, the extensor and flexor tibiae. A variety of sense organs on and in each leg provide feedback about this joint's position and movement and about forces acting on the exoskeleton and muscles. One such organ is a muscle tension receptor found within the flexor tibiae muscle of the mesothoracic leg. We now show that an apparently homologous multipolar receptor is present in the hind leg, but that here it is associated with a specialised flexor muscle, the accessory flexor. This muscle comprises 13 fibres, innervated by five of the thirteen motor neurones that innervate the main flexor muscle and, since these are slow motor units, the response properties of the receptor are constrained. The multipolar receptor attaches to the muscle fibres near their proximal insertion onto the femoral cuticle. It generally has four primary dendrites, which do not branch extensively within the muscle. We show that the receptor responds strongly to active, isometric contractions but only poorly to imposed changes of accessory flexor muscle length (i.e. passive changes in tibial position). It does not respond to tension generated by the main flexor muscle or by the extensor muscle. The tension receptor causes short-latency (0.9­1.8 ms) excitatory inputs onto the three common inhibitory motor neurones and longer-latency (3.7­8.1 ms) inhibitory inputs onto the slow extensor tibiae motor neurone. In quiescent animals, it causes excitatory inputs onto flexor tibiae motor neurones (2.2­3.8 ms) but, in more active animals, its inputs onto these neurones are often inhibitory, with delays of 6­10 ms. The slow nature of the accessory flexor muscle and the pattern of central connections of the receptor suggest that together they are involved in the control of slow movements or posture, potentially acting through a servomechanism.