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 unresolved. Applying the CRISPR/Cas9-mediated split-GFP tagging, we visualized the endogenous active zone scaffold protein, Bruchpilot (Brp), in specific cells. This technology enabled the spatial characterization of presynaptic machineries only within the Kenyon cells (KCs) of the Drosophila mushroom bodies. We found the patterned accumulation of Brp among the compartments of axon terminals, where a KC synapses onto different postsynaptic neurons. Mechanistically, the localized octopaminergic modulation along {gamma} KC terminals regulate this compartmental Brp heterogeneity via Oct{beta}2R and cAMP signaling. We further found that acute food deprivation reorganizes this spatial pattern in an octopamine-dependent manner. Such coordinated regulation of local synaptic machineries thus explains how the mushroom bodies integrate changing physiological states. This subcellular information processing represents an elegant solution to expand computational capacity of the circuit.