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From genes to behavior: genetic dissection of visual circuitry using Drosophila melanogaster

Subject Area Molecular Biology and Physiology of Neurons and Glial Cells
Term from 2016 to 2021
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 269962750
 
Final Report Year 2024

Final Report Abstract

The visual system of the vinegar fly Drosophila melanogaster has long served as one of the best understood model systems in developmental genetics. Over the past decades, Drosophila also became an important model for understanding how neural circuits guide visual perception on a cellular and synaptic level. Especially the study of short visual fiber photoreceptors R1-6 and their post-synaptic targets in the optic lobes was crucial for understanding how direction selectivity arises in a neural circuit computing visual motion. At the beginning of this project, far less was known about the function and connectivity of long visual fiber photoreceptors R7 and R8, whose molecular and morphological features define three distinct ommatidial subtypes, named ‘pale’, yellow, and DRA. A stochastic retinal mosaic formed throughout 95% of the adult fly retina is formed by pale & yellow ommatidia, with R7 and R8 expressing different combinations of Rhodopsin genes, and is ideally suited for serving color vision. The remaining ~5% of ommatidia form a narrow band along the dorsal head cuticle (the so-called ‘dorsal rim area’, or DRA) with R7 and R8 forming monochromatic pairs of skylight polarization sensors with enlarged rhabdomere diameters and orthogonally aligned, untwisted microvilli orientations. Outside the DRA region, the distal medulla cell type Dm8 had been identified as the strongest post-synaptic target of UV-sensitive R7 cells, pooling inputs from ~14 neighboring facets and thereby being ideally suited as a key circuit motif for coloropponent processing. When we started, nothing was known about potential similarities or differences between circuits for processing color versus skylight polarization. Could the same circuit Bauplan compute both stimuli? Of would modality-specific adaptations be necessary? We used a combination of neuroanatomical tools and behavior experiments for investigating DRA circuitry. On one hand, we built virtual flight arenas for quantifying navigational decisions of tethered flies (wither wild type or upon manipulation of circuit function). On the other hand, we used state-of-the-art light microscopic techniques to systematically characterize DRA circuit elements. About half way through the project, newly available EM-based connectomics data could be accessed to investigate synaptic connectivity. To our surprise, we found two distinct Dm8-like cell types only in the DRA, post-synaptic to either R7-DRA (Dm-DRA1), or to R8-DRA (Dm-DRA2). Such a duplication of R7→Dm8 circuitry is well suited for processing orthogonal angles of polarization with equal weights. Finally, we described different classes of visual projection neurons (called MeTu cells), some of which were specifically downstream of Dm-DRA1 and therefore serve as the gateway for skylight polarization information into the central complex.

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