Abstract

BackgroundTopographic maps form the basis of neural processing in sensory systems of both vertebrate and invertebrate species. In the Drosophila visual system, neighboring R1–R6 photoreceptor axons innervate adjacent positions in the first optic ganglion, the lamina, and thereby represent visual space as a continuous map in the brain. The mechanisms responsible for the establishment of retinotopic maps remain incompletely understood.ResultsHere, we show that the receptor Golden goal (Gogo) is required for R axon lamina targeting and cartridge elongation in a partially redundant fashion with local guidance cues provided by neighboring axons. Loss of function of Gogo in large clones of R axons results in aberrant R1–R6 fascicle spacing. Gogo affects target cartridge selection only indirectly as a consequence of the disordered lamina map. Interestingly, small clones of gogo deficient R axons perfectly integrate into a proper retinotopic map suggesting that surrounding R axons of the same or neighboring fascicles provide complementary spatial guidance. Using single photoreceptor type rescue, we show that Gogo expression exclusively in R8 cells is sufficient to mediate targeting of all photoreceptor types in the lamina. Upon lamina targeting and cartridge selection, R axons elongate within their individual cartridges. Interestingly, here Gogo prevents bundling of extending R1-6 axons.ConclusionTaken together, we propose that Gogo contributes to retinotopic map formation in the Drosophila lamina by controlling the distribution of R1–R6 axon fascicles. In a later developmental step, the regular position of R1–R6 axons along the lamina plexus is crucial for target cartridge selection. During cartridge elongation, Gogo allows R1–R6 axons to extend centrally in the lamina cartridge.

Highlights

  • Precise wiring of the visual system enables animals to perceive and respond to their visual world

  • We found that the lamina map forms by using a combination of mechanisms that directly and indirectly depend on the transmembrane receptor Golden goal (Gogo), previously described as mediating R8 targeting in the medulla [18,19]

  • Single cell mosaic analysis with a repressible cell marker (MARCM) experiments for R1–R6 axons were performed using a heat shock FLP recombinase. 3rd instar larvae were heat shocked for 1 h at 38uC and neurons were labeled by expressing UAS-mCD8GFP under the control of the pan-neuronal driver elav-Gal4

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Summary

Introduction

Precise wiring of the visual system enables animals to perceive and respond to their visual world. In Drosophila, axons project in a topographic fashion, such that adjacent photoreceptor (R) cells connect to adjacent postsynaptic neurons [1,2]. Many studies in vertebrates and invertebrates revealed molecular mechanisms controlling precise columnar and layer-specific axon targeting during visual system development [3,4,5,6,7,8,9,10,11]. In the Drosophila visual system, it is thought that targeting of R cells follows a genetically hard-wired program to form complex and stereotyped microcircuits [12]. In the Drosophila visual system, neighboring R1–R6 photoreceptor axons innervate adjacent positions in the first optic ganglion, the lamina, and thereby represent visual space as a continuous map in the brain. The mechanisms responsible for the establishment of retinotopic maps remain incompletely understood

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