The ability of animals to navigate their environment, locate food sources, and find mating partners hinges on their capacity to process and integrate information provided by the visual system. At the heart of this complex task lies the intricate web of thousands of individual neurons, each playing a crucial role in the orchestration of sensory information. Understanding the rules and mechanisms guiding this neural computation is a profound pursuit central to the fields of neuroscience and ethology. My doctoral research advances our understanding of navigation by delving into neural circuitry and information processing mechanisms, particularly emphasizing polarized skylight detection in insects. Focused on Drosophila melanogaster, a powerful model organism, the study explores the intricate visual system comprised of optically isolated unit eyes called ommatidia. Approximately 800 of these units populate the adult retina, facilitating precise spatial sampling. Within the Drosophila retina, different ommatidial subtypes house specialized inner photoreceptors for color perception in the central retina or the detection of skylight polarization in the dorsal rim area (DRA). Visual information undergoes complex processing in the optic lobes before being relayed to higher brain structures, such as the anterior optic tubercle (AOTU) within the visual glomeruli. My thesis contributes to understanding the less well-known ventral polarization vision, exploring local circuitries in the optic lobes, and shedding light on the less-understood aspect of this visual modality. The literature study identifies functionally specialized non-DRA detectors by examining non-celestial polarization vision across diverse insect species, including dragonflies, butterflies, beetles, bugs, and flies. Although the ventral polarization vision in Drosophila melanogaster presents a fascinating modality, the unknown location of the specific circuitry stays hidden. Therefore, I turned my attention to the better-known specific circuitry of skylight polarization vision in the DRA and unveiled modality-specific connectivities of local medulla neurons in the DRA. Including Mt11-like medulla tangential cells that avoid the DRA region. Despite gathering comprehensive information from the entire medulla, these cells lack inputs related to polarized light from the DRA, indicating separate processing of distinct visual attributes within the central brain. Finally, I characterized the anatomical and physiological properties of MeTu-types, modality-specific to the DRA, called MeTu-DRA1 and MeTu-DRA2. Using the genetic toolkit of Drosophila melanogaster, the study showed for the first time that both populations are modality-specific postsynaptic to DRA.R7 photoreceptors only, project to the same subunit of the AOTU and show differences in their morphology as well as connectivity. Although the morphology showed significant differences, single-cell clones revealed a topographic projection of both MeTu-DRA sub-populations from the medulla to the AOTU. Based on these findings, we hypothesized that the anatomical and connectivity differences might result in different physiological response patterns of MeTu-DRA1 and MeTu-DRA2. In order to test this theory, I implemented calcium imaging (using GCaMP) under a 2-photon microscope. I recorded the physiological response properties of Dm-DRA1 (in the medulla) and MeTu-DRA1 and MeTu-DRA2 responses in the AOTU. Interestingly, I could show for the first time that MeTu-DRA1 shows a detailed representation of different ’Angle of Polarization’ (AoP) in the AOTU, and MeTu-DRA2 responses, however, split the AOTU in a dorsal or ventral half pattern. With EM reconstruction, we could identify a more detailed circuitry of the MeTu-DRAs and a new DRA-specific interhemispheric cell type called MeMe-DRAs. Additionally, I could show that only MeTu-DRA2 responds to unpolarized UV flashes presented contralaterally, which is most likely mediated by MeMe-DRAs and presents an early binocular integration of polarized skylight information. In conclusion, the discoveries made during my doctoral research significantly contribute to our comprehension of the functional characteristics and circuitry of MeTu-DRA neurons in . This comprehensive understanding enhances our knowledge of how binocular integration plays a crucial role in the neural mechanisms guiding polarization vision and navigation.
