Functional stratification of sensory encoding in a biological gyroscope

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Flying insects are among the most maneuverable animals on the planet, and must rapidly integrate information from multiple senses to achieve fine-scale control of locomotion. For example, flies combine input from the eyes and small, dumbbell-shaped structures known as halteres to both maintain stability and perform aerial maneuvers. The halteres are located behind the forewings and evolved from the hindwings. The halteres are well-known as biological gyroscopes, detecting body rotations that in turn trigger a number of stabilization reflexes, including changes in wing motion. At their base, the halteres possess hundreds of biological strain gauges, known as campaniform sensilla, that provide the wing steering muscles with direct feedback each wingstroke. Recent evidence suggests that the haltere is under active control during flight, making it a multifunctional sensory organ that helps flies perform maneuvers and still maintain their balance while in the air. However, how the haltere accomplishes these dual roles, and how these roles relate to the activity of the wing muscles, remains unclear. A more complete understanding of the haltere’s role in flight control will provide insight into how this unique sensory organ endows flies with their exquisite flight capacities. This project involves a collaboration with the Morehead Planetarium that takes advantage of the principal investigator’s extensive experience in informal education to foster public dialogue through Carolina Science Cafés. Additionally, undergraduates from underrepresented groups will be mentored in conducting research throughout this project. Finally, the results from this research will help develop micro air vehicles navigate complex environments.The goal of this proposal is to reveal the principles of sensory encoding and sensorimotor processing that flies use in controlling the haltere, and thus, their aerial maneuvers. The research will focus on the fruit fly, Drosophila melanogaster, and combine new in vivo imaging techniques with analysis approaches drawn from computational neuroscience and muscle electrophysiology. Through expression of the genetically-encoded, optical calcium sensor GCaMP, the activity of haltere campaniform sensilla during visually-guided flight maneuvers will be directly observed. These experiments will test the hypothesis that specific regions of the haltere encode different aspects of visual motion, such as direction or angular velocity. Then, reverse correlation analysis will be used to construct quantitative models that test if these different regions are recruited in a linear or nonlinear fashion during active maneuvers. Finally, simultaneous calcium imaging and electrophysiology of the wing steering muscles will address if the functional divisions of the wing muscles are derived from particular regions of the haltere. Furthermore, this work will demonstrate how the arrangement and location of mechanosensors acts as a filter for behaviorally relevant stimuli. By taking an organismal approach, and linking the micromechanics of sensory structures with flight behavior, these experiments will make clear the selective pressures that led to the haltere’s evolution.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.