The fast extensor tibiae motor neuron makes direct excitatory central connections with the posterior group of flexor tibiae motor neurons in the locust metathoracic ganglion. The flexor group has a slow, a fast, and an intermediate motor neuron. The motor neurons are involved in the motor program for kicking and jumping, the defensive and escape behaviors of the locust. An antidromic action potential in fast extensor tibiae motor neuron (FETi) results in a monosynaptic, glutamatergic excitatory postsynaptic potential (EPSP) in each of the flexor motor neurons. 2. A train of 10 antidromic spikes in FETi at frequencies of 1-20 Hz resulted in depression of the amplitude of the EPSP in each of the flexor motor neurons. The depression was not significantly different in the different flexor motor neurons. The depression was greater with higher frequency stimulation and was reduced in low calcium saline. 3. After stimulation at 20 Hz, the EPSP amplitude was depressed by approximately 80%. This did not change when the number of stimuli was increased to 20, when stimulation was done in high calcium saline, or when the frequency of stimulation was increased to 50 or 100 Hz. The recovery from depression was greater after 20-Hz stimulation than at lower frequencies, although the recovery was reduced when the number of stimuli was increased, and also in high calcium saline. 4. In normal saline the depression of the EPSP amplitude was associated with a reduction of the presynaptic spike amplitude at frequencies of > or = 5 Hz. In tetraethylammonium (TEA) saline the width of a TEA-broadened spike was also reduced. The reduction in spike amplitude and spike width correlated with the depression of the EPSP. 5. Certain of these results are consistent with a depletion model of synaptic depression, whereas others are not consistent with this model. The depression may be partly due to an initial depletion of transmitter stores, and partly to modulation of the presynaptic action potential that reduces calcium entry, and therefore transmitter release. The significance of the depression on the motor program for kicking and jumping is discussed.
