Key resources used in this study.

Neurons can adjust synaptic output according to the postsynaptic partners. However, the target-specific regulation of 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 the presynaptic scaffolds 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 projections along γ KC terminals regulate this compartmental Brp heterogeneity via Octβ2R and cAMP signaling. We further found that physiological stress, such as food or sleep deprivation reorganizes this intracellular pattern in an octopamine-dependent manner. Such concurrent regulation of local active zone assemblies thus suggests how the mushroom bodies integrate changing physiological states.