Octopamine signals coordinate the spatial pattern of presynaptic machineries within individual Drosophila mushroom body neurons

Neurons need to adjust synaptic output according to the targets. However, the target-specific synaptic structures within individual neurons in the central nervous system remains largely unresolved, due to the high density of neuropils. Applying the CRISPR/Cas9-mediated split-GFP tagging, we devised cell-type specific fluorescent visualization of the endogenous active zone scaffold protein, Bruchpilot (Brp). This technology enabled the spatial characterization of presynaptic machineries within the Kenyon cells of the Drosophila mushroom bodies. We found the patterned accumulation of Brp among the compartments of axon terminals, where a Kenyon cell synapse onto different neurons. Mechanistically, the localized octopaminergic signaling along Kenyon cell terminals regulate this compartmental Brp heterogeneity via Oct(2R and cAMP signaling. We further found that acute food deprivation reorganizes this spatial pattern in an octopaminergic signaling-dependent manner. Such coordinated regulation of local synaptic machineries thus explains how the mushroom bodies integrate changing physiological states.