Local Specification of Relative Strengths of Synapses between Different Abdominal Stretch-Receptor Axons and their Common Target Neurons

Stretch-receptor (SR) axons form a parallel array of 20 excitatory synapses with target neurons in the crayfish CNS. In each postsynaptic neuron, EPSPs from different SR axons differ significantly in size. These amplitudes are correlated with the segment in which each axon originates and form a segmental gradient of synaptic excitation in individual postsynaptic neurons. These differences might arise postsynaptically because of differential postsynaptic attenuation or presynaptically because of local regulation of the strength of each synapse. To examine these possibilities, we stimulated each SR axon separately and studied integration of its EPSPs in an identified neuron, Flexor Inhibitor 6 (FI6). Transmission from SR axons to FI6 was chemical and direct: EPSPs were accompanied by an increased postsynaptic conductance, were affected by extracellular Ca(2+), and showed frequency-dependent depression. EPSPs from different SR axons summed linearly. The rise times of EPSPs from different SR axons were not significantly different. We also filled individual SR axons and FI6 neurons and mapped and counted their points of contact. Each SR axon contacted each FI6 bilaterally, and contacts of SR axons from different segments were intermingled on FI6. SR axons that made the strongest synapses made more points-of-contact with FI6. These results imply that differences in strength do not arise because of differential postsynaptic attenuation of EPSPs, but rather because certain SR axons predictably make more points of contact with FI6 than do others. Thus, this gradient in excitation requires that each synapse be regulated by an exchange between the SR axon and its target neuron.