Compartmentalization of central neurons in Drosophila: a new strategy of mosaic analysis reveals localization of presynaptic sites to specific segments of neurites.

Synaptogenesis in the CNS has received far less attention than the development of neuromuscular synapses, although only central synapses allow the study of neuronal postsynaptic mechanisms and display a greater variety of structural and functional features. This neglect is attributable mainly to the enormous complexity of the CNS, which makes the visualization of individual synapses on defined neuronal processes very difficult. We overcome this obstacle and demonstrate by confocal microscopy the specific arrangement of output synapses on individual neurites. These studies are performed via genetic mosaic strategies in the CNS of the fruitfly Drosophila melanogaster. First, we use targeted expression of synaptic proteins by the UAS/Gal4 system. Second, we apply a newly developed transplantation-based mosaic strategy that takes advantage of the intrinsic regulation and localization of synaptic proteins in single-cell clones. We propose the existence of three distinct neuritic compartments: (1) primary neurites that appear to form the main transport pathways and are mostly void of output synapses, (2) neuritic compartments that contain output synapses, and (3) neuritic compartments that are postsynaptic in nature. In addition we show that mutations of the kakapo gene have no obvious effect on the distribution of output synapses in the CNS, whereas neuromuscular synapses are severely reduced. This suggests that synaptogenic mechanisms in the CNS might differ from those at neuromuscular junctions.