Divergent short-term plasticity creates parallel pathways for computation and behavior in an olfactory circuit

To enable diverse sensory processing and behavior, central circuits use divergent connectivity to create parallel pathways. However, linking subcellular mechanisms to the circuit-level segregation of computation has been challenging. Here, we investigate the generation of parallel processing within a divergent network in the Drosophila olfactory system, where single projection neurons target multiple types of lateral horn neuron (LHN). One LHN type generates sustained responses and adapts divisively to encode temporal odor contrast. The other generates transient responses and adapts subtractively to encode a form of positive temporal prediction error. These coding differences originate from subcellular differences in short-term plasticity in projection neuron axons. Prediction error arises from strongly facilitating synapses, which depend on the presynaptic priming factor Unc13B. The temporal contrast code arises from mildly depressing synapses that engage additional gain control implemented by the Na+/K+ ATPase in the postsynaptic neuron. Each LHN type makes corresponding dynamic contributions to behavioral odor attraction. Subcellular synaptic specialization is a compact and efficient way to generate diverse parallel information streams.