Synaptic Dynamics Convey Differential Sensitivity to Input Pattern Changes in Two Muscles Innervated by the Same Motor Neurons.

Postsynaptic responses depend on input patterns as well as short-term synaptic plasticity, summation, and postsynaptic membrane properties, but the interactions of those dynamics with realistic input patterns are not well understood. We recorded the responses of the two pyloric dilator (PD) muscles, and , that are innervated by and receive identical periodic bursting input from the same two motor neurons in the lobster and showed quantitative differences in membrane nonlinearities and synaptic summation. At a short timescale, responses in both muscles were dominated by facilitation, albeit with different frequency and time dependence. Realistic burst stimulations revealed more substantial differences. Across bursts, showed transient depression, whereas showed transient facilitation. Steady-state responses to bursting input also differed substantially. Neither muscle had a monotonic dependence on frequency, but showed particularly pronounced bandpass filtering. was sensitive to changes in both burst frequency and intra-burst spike frequency, whereas, despite its much slower responses, was largely insensitive to changes in burst frequency. was sensitive to both burst duration and number of spikes per burst, whereas was sensitive only to the former parameter. Neither muscle showed consistent sensitivity to changes in the overall spike interval structure, but was surprisingly sensitive to changes in the first intervals in each burst, a parameter known to be regulated by dopamine (DA) modulation of spike propagation of the presynaptic axon. These findings highlight how seemingly minor circuit output changes mediated by neuromodulation could be read out differentially at the two synapses.