Selective adhesion preserves eye patterning as axonal retinotopy in the Drosophila brain

Flies, like vertebrates, preserve the spatial organization of visual input through axonal projections into the brain, a principle called retinotopy. The best-known developmental mechanisms for retinotopy are molecular gradients in the target regions, yet Drosophila photoreceptors can form retinotopic maps ectopically in wrong brain regions. We show that a temporal gradient of axonal growth plus selective adhesion between photoreceptor axons precisely preserves the cellular eye pattern. Each of the 800 single eyes, the ommatidia, form a bundle of six axons that are held in place by inter-bundle adhesion through the protocadherin Flamingo and preserve their intra-bundle organization through the adhesion molecule Sidekick. Computational modeling of axon terminals as selectively adhesive soft bodies in a developmental wave generates the retinotopic pattern, including the shapes of the postsynaptic lamina neurons, which emerge without explicit encoding. Hence, a temporal gradient and two adhesive forces can ensure retinotopic map formation without a target-derived mechanism. VIDEO ABSTRACT.