Axon arrival times and physical occupancy establish visual projection neuron integration on developing dendrites in the Drosophila optic glomeruli

Abstract

Behaviorally relevant, higher order representations of an animal’s environment are built from the convergence of visual features encoded in the early stages of visual processing. Although developmental mechanisms that generate feature encoding channels in early visual circuits have been uncovered, relatively little is known about the mechanisms that direct feature convergence to enable appropriate integration into downstream circuits. Here we explore the development of a collision detection sensorimotor circuit in Drosophila melanogaster , the convergence of visual projection neurons (VPNs) onto the dendrites of a large descending neuron, the giant fiber (GF). We find VPNs encoding different visual features establish their respective territories on GF dendrites through sequential axon arrival during development. Physical occupancy, but not developmental activity, is important to maintain territories. Ablation of one VPN results in the expansion of remaining VPN territories and functional compensation that enables the GF to retain responses to ethologically relevant visual stimuli. GF developmental activity, observed using a pupal electrophysiology preparation, appears after VPN territories are established, and likely contributes to later stages of synapse assembly and refinement. Our data highlight temporal mechanisms for visual feature convergence and promote the GF circuit and the Drosophila optic glomeruli, where VPN to GF connectivity resides, as a powerful developmental model for investigating complex wiring programs and developmental plasticity.