Sensorimotor Transformations for Controlling Heading Direction in the Insect Central Complex

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Survival of an organism relies on its ability to navigate through a complex environment. During navigation, the nervous system integrates spatial information from a wide variety of sensory modalities into a stable heading direction. In insects, such as the fruit fly Drosophila melanogaster, this process takes place in the central complex, a series of neuropil structures in the brain. A hallmark of the central complex is its columnar organization, in which neuronal activity appears as stable bumps that correlate with changes in the organism’s heading direction. The Drosophila central complex has been the subject of extensive anatomical and functional characterization, which has revealed how sensory percepts are transformed through its various compartments. However, the understanding of how neuronal activity in the central complex is translated into behavior is strictly correlational. To establish a causal relationship between central complex activity and heading direction, a thorough behavioral dissection is required. Further, the circuits that relay central complex activity to motor command centers are still poorly understood. Our proposal details a comprehensive research plan to optogenetically manipulate the inputs and outputs of the Drosophila fan-shaped body (FB), a key structure in the central complex. These manipulations will reveal the contributions of the FB input and output neurons to generating a heading direction. To achieve this, we developed a behavior chamber for tracking locomotion of walking flies during optogenetic manipulations. We use this chamber to activate FB neurons in different sensory contexts. Additionally, we will map how outputs from the central complex are routed to command centers in the brain. To this end, we will employ various new configurations of trans-Tango, the transsynaptic circuit mapping and manipulation technique developed by our laboratory. The first of these is trans-Tango(behavior), which allows selective optogenetic manipulation of the postsynaptic partners of a chosen starting population. The second is ds-Tango, a method for mapping neurons mono- and di-synaptic to a chosen starter population. The final is retro-Tango, a transsynaptic mapping tool that works in the retrograde direction. Our studies will reveal how spatial information of sensory cues is translated through multiple layers of circuitry to elicit the navigational drive. Our results will, therefore, represent a key step forward in the knowledge of how the nervous system transforms sensory information into behavior. Finally, our studies will reveal circuit motifs in insects that may be conserved in mammals to perform analogous functions. Therefore, the circuits we describe in insects may contribute to the understanding of spatial perception in humans, one of the first cognitive faculties impacted in Alzheimer's disease.