An excitatory connection between an extensor and several flexor tibiae motor neurons that innervate antagonistic muscles in the hind leg of a locust has been characterized using physiological and ultrastructural methods. Simultaneous intracellular recordings from the single fast extensor (FETi) motor neuron and up to three flexor motor neurons show that a spike in FETi is followed by a short latency depolarizing synaptic potential in the flexors that is powerful enough to evoke a burst of flexor spikes. The chemically mediated excitatory postsynaptic potential (EPSP) is caused centrally as it persists when sensory feedback from the leg is removed, and has a latency of 1.6–2.0 ms depending upon the position of the recording electrodes in the somata or neuropilar segments of the pre- and postsynaptic neurons. The amplitude of the EPSP declines gradually in a saline containing no calcium but high magnesium, indicating that no spiking interneuron is interposed in the pathway. With repetitive stimulation, the EPSP decrements markedly so that at intervals of 50 ms the second EPSP of a pair is reduced by 90%. The amplitude of the EPSP is also dependent on the amplitude of the presynaptic spike.
The physiological evidence suggesting a monosynaptic connection is directly confirmed by electron microscopy of ganglia in which FETi and a flexor were both labelled with horseradish peroxidase. Direct chemical synapses between the two identified neurons, in which FETi is the presynaptic element, occur in three regions of the neuropil examined. At a synapse, the flexor motor neuron may be the only postsynaptic neuron or it may be one element in a dyad. The synaptic arrangements between the two neurons are complex with serial synapses through unlabelled processes linking FETi to flexor motor neurons and with frequent reciprocal synaptic connections between FETi and unlabelled processes. Unidentified processes also make input synapses on both neurons close to the synapses from FETi.
The behavioural significance of the connection lies in the mechanical requirements for kicking and jumping. To prepare for these powerful movements the extensor and flexor tibiae muscles must co-contract. The connection from FETi enhances the depolarization and frequency of spikes in the flexors during the co-contraction.