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Linking neural circuits to visual guidance in flying flies

Final Report Summary - FLYVISUALCIRCUITS (Linking neural circuits to visual guidance in flying flies)

In the project FlyVisualCircuits, we made several notable accomplishments. First were the technological accomplishments. To realize the scientific goals of the project, we made extensive developments to virtual reality systems for freely moving animals. The particular novelty of this system is the ability to place animals, completely unrestrained and not physically modified in any way, into a dynamic, reactive, immersive 3D virtual world. We validated the system's effectiveness on multiple species, namely flies, fish and mice, and the work is the subject of strong interest from other scientists and the general public. This VR system called "FreemoVR" and its precursors were published in key scientific papers and were made available as free open source software. Furthermore, former project members founded a startup company that sells services based on multiple aspects of this technology and multiple collaborations were started based on this technology. In addition to our own scientific work within the project using this technology (described below), we demonstrated novel experimental capabilities with this system which will be useful in the fields of neuroscience, animal behavior, and ecology. Because the system operates on freely moving animals but is capable of simulating realistic visual surroundings, it will be useful for studying the neurobiology and behavior of navigation. Historically such studies have had to choose between rigorously controlled experiments on restrained animals which, due to the restraint, may result in unnatural neural or behavioral responses. Alternatively, freely moving animals may have naturalistic stimulation but with reduced ability to stimulate or record precisely. The FreemoVR system allows freely moving animals to be stimulated with precise, experimenter defined visual stimuli. Combined with recent electrophysiological and optophysiological technologies to enable recordings in freely moving animals, the technology offers new experimental possibilities for research into navigation in species including rodents, fish and insects. In addition to the technology's novel prospects for studying animal navigation, we also demonstrated the ability to dynamically control interaction between real and virtual animals. This ability - to place real and virtual animals in the same space - solves a major technical challenge faced by scientists trying understand visually mediated collective behavior by introducing the ability to control interactions between individuals with a computer program. Further technical achievements included the development of a system for using opto- and thermo-genetics to control neural activity of freely moving Drosophila.

Scientifically, we made use of these new technologies to investigate the neural circuits underlying visually guided locomotion in Drosophila. We discovered that a ubiquitous phenomenon in biological motion detection - asymmetric responses to motion - gives rise in simplified models to phenomena which have been observed in behavioral experiments from many labs over many decades. For example, wide-field motion detecting neurons such as the lobula plate tangential cells are known to respond asymmetrically. That is, motion in the preferred direction creases larger amplitude depolarization than motion in the null direction causes hyperpolarization. Model flies with a visual system composed of only such asymmetric wide-field motion detectors are capable of turning towards visual objects, a phenomenon previously argued to require use of additional circuitry. Thus, we have shown how known circuits may serve a greater range of behavior than previously realized. In additional work, we made a neuro-anatomical description of the Drosophila optic glomeruli and the neurons projecting to these important visual brain regions. This work was performed by using a novel approach that identifies brain compartments based on expression patterns of genomic sequences corresponding to putative transcriptional enhancers.