A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor

Abstract

The chordotonal organ at the femorotibial joint of a locust hind leg monitors extension and flexion movements of the tibia. During evoked or imposed movements of this joint the central terminals of afferent neurons from the chordotonal organ receive depolarizing, inhibitory synaptic inputs. The afferent spikes are therefore superimposed on these depolarizing IPSPs, which are generated indirectly by other afferents from the same organ that respond to the same movement. Each afferent spikes preferentially to particular features of a joint movement, and its synaptic input is typically greatest at the joint position or during the movement that generates its best response. Afferents that respond to only one direction of movement receive synaptic inputs either during movements in both directions, or only during movements in their preferred direction. Phasic velocity-sensitive afferents receive either phasic inputs during movements, or tonic inputs at new sustained joint positions, or both. The spikes of tonic position-sensitive afferents are superimposed on synaptic inputs that are dependent on joint position. The synaptic inputs sum but do not themselves evoke antidromic spikes in the afferent terminals. They reduce the amplitude of orthodromic afferent spikes by 12-28%, and this is accompanied by a reduction of up to 50% in the amplitude of monosynaptic EPSPs evoked by an afferent in postsynaptic leg motor neurons. These interactions suggest that a local gain control mechanism operates between the afferents of this proprioceptor. Thus, the effectiveness of the output synapses of an individual afferent is regulated by the network action of other chordotonal afferents that respond to the same movement.