Neural circuits underlying colour vision and visual memory in Drosophila melanogaster

Focusing at the fly visual system I am addressing the identity and function of neurons accomplishing two fundamental processing steps required for survival of most animals: neurons of peripheral circuits underlying colour vision as well neurons of higher order circuits underlying visual memory. Colour vision is commonly assumed to rely on photoreceptors tuned to narrow spectral ranges. In the ommatidium of Drosophila, the four types of so-called inner photoreceptors express different narrow-band opsins. In contrast, the outer photoreceptors have a broadband spectral sensitivity and are thought to exclusively mediate achromatic vision. Using computational models and behavioural experiments, I here demonstrate that the broadband outer photoreceptors contribute to colour vision in Drosophila. A model of opponent processing that includes the opsin of the outer photoreceptors scores the best fit to wavelength discrimination behaviour of flies. To experimentally uncover the contribution of individual photoreceptor types, I used blind flies with disrupted phototransduction (norpA-) and rescued norpA function in genetically targeted photoreceptors and receptor combinations. Surprisingly, dichromatic flies with only broadband photoreceptors and one additional receptor type can discriminate different colours, indicating the existence of a specific output comparison of outer and inner photoreceptors. Furthermore, blocking interneurons postsynaptic to the outer photoreceptors specifically impairs colour but not intensity discrimination. These findings show that outer receptors with a complex and broad spectral sensitivity do contribute to colour vision and reveal that chromatic and achromatic circuits in the fly share common photoreceptors. Higher brain areas integrate sensory input from different modalities including vision and associate these neural representations with good or bad experiences. It is unclear, however, how distinct sensory memories are processed in the Drosophila brain. Furthermore, the neural circuit underlying colour/intensity memory in Drosophila remained so far unknown. In order to address these questions, I established appetitive and aversive visual learning assays for Drosophila. These allow contrasting appetitive and aversive visual memories using neurogenetic methods for circuit analysis. Furthermore, the visual assays are similar to the widely used olfactory learning assays and share reinforcing stimuli (sugar reward and electric shock punishment), conditioning regimes and methods for memory assessment. Thus, a direct comparison of the cellular requirements for visual and olfactory memories becomes feasible. I found that the same subsets of dopamine neurons innervating the mushroom body are necessary and sufficient for formation of both sensory memories. Furthermore, expression of D1-like Dopamine Receptor (DopR) in the mushroom body is sufficient to restore the memory defect of a DopR null mutant (dumb-). These findings and the requirement of the mushroom body for visual memory in the used assay suggest that the mushroom body is a site of convergence, where representations of different sensory modalities may undergo associative modulation.