Positive feedback loops from proprioceptors involved in leg movements of the locust

Summary

• 1. Two campaniform sensilla (CS) on the proximal tibia of a hindleg monitor strains set up when a locust prepares to kick, or when a resistance is met during locomotion. The connections made by these afferents with interneurones and leg motor neurones have been investigated and correlated with their role in locomotion.

• 2. When flexor and extensor tibiae muscles cocontract before a kick afferents from both campaniform sensilla spike at frequencies up to 650 Hz. They do not spike when the tibia is extended actively or passively unless it encounters a resistance. The fast extensor tibiae motor neurone (FETi) then produces a sequence of spikes in a thrusting response with feedback from the CS afferents maintaining the excitation. Destroying the two campaniform sensilla abolishes the re-excitation of FETi.

• 3. Mechanical stimulation of a single sensillum excites extensor and flexor tibiae motor neurones. The single afferent from either CS evokes EPSPs in the fast extensor motor neurone and in certain fast flexor tibiae motor neurones which follow each sensory spike with a central latency of 1.6 ms that suggests direct connections. The input from one receptor is powerful enough to evoke spikes in FETi. The slow extensor motor neurone does not receive a direct input, although it is excited and slow flexor tibiae motor neurones are unaffected.

• 4. Some nonspiking interneurones receive direct connections from both afferents in parallel with the motor neurones. One of these interneurones excites the slow and fast extensor tibiae motor neurones probably by disinhibition. Hyperpolarization of this interneurone abolishes the excitatory effect of the CS on the slow extensor motor neurone and reduces the excitation of the fast. The disinhibitory pathway may involve a second nonspiking interneurone with direct inhibitory connections to both extensor motor neurones. Other nonspiking interneurones distribute the effects of the CS afferents to motor neurones of other joints.

• 5. The branches of the afferents from the campaniform sensilla and those of the motor neurones and interneurones in which they evoke EPSPs project to the same regions of neuropil in the metathoracic ganglion.

• 6. The pathways described will ensure that more force is generated by the extensor muscle when the tibia is extended against a resistance. The excitatory feedback to the extensor and flexor motor neurones will also contribute to their co-contraction when generating the force necessary for a kick.