Divergent synaptic dynamics originate 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 synaptic and cellular mechanisms to the circuit-level segregation of computation has been challenging. Here, we investigate the generation of parallel processing pathways in the Drosophila olfactory system, where glomerular projection neurons (PNs) diverge onto many lateral horn neurons (LHNs). We compare the effects of a single PN's activity on two of its target LHNs. One LHN type generates sustained responses to odor and adapts divisively. The other generates transient responses and adapts subtractively. The distinct odor-coding dynamics originate from differences in the dynamics of PN synapses targeting each LHN type. Sustained LHN responses arise from synapses that recover from depression quickly enough to maintain ongoing transmission. Divisive adaptation is due to slow cellular gain control implemented by the Na⁺/K⁺ ATPase in the postsynaptic neuron. Transient LHN responses arise from synapses that recover from depression too slowly to maintain ongoing transmission but that also facilitate when PN spike rate increases. Interfering with facilitation via the calcium buffer EGTA or interfering with the presynaptic priming factor Unc13B diminishes the magnitude of initial transient responses. Subtractive adaptation is due to the nonlinearity imposed by the spike threshold in the postsynaptic neuron. Transient LHNs make corresponding transient contributions to behavioral odor attraction in walking flies, whereas sustained LHNs may make sustained, but nuanced, contributions. Subcellular presynaptic specialization is thus a compact and efficient way to originate parallel information streams for specialized computation and behavior.