Functional stratification of sensory encoding in a biological gyroscope

飞行昆虫是地球上最具机动性的动物之一，它们必须迅速整合来自多个感官的信息，才能实现对运动的精细控制。例如，苍蝇将眼睛的输入和被称为笼头的小哑铃状结构结合在一起，既保持稳定，又进行空中机动。吊环位于前翼后面，由后翼进化而来。吊环是众所周知的生物陀螺仪，它探测身体的旋转，进而触发一些稳定反射，包括机翼运动的变化。在它们的底部，笼头有数百个生物应力计，被称为钟状感受器，为翅膀的操纵肌提供每一次击打翅膀的直接反馈。最近的证据表明，吊环在飞行过程中处于主动控制之下，使其成为一种多功能感官器官，帮助苍蝇在空中进行动作并保持平衡。然而，笼头如何完成这两个角色，以及这些角色如何与翅膀肌肉的活动相关，目前仍不清楚。更全面地了解吊灯在飞行控制中的作用，将有助于深入了解这种独特的感官器官是如何赋予苍蝇出色的飞行能力的。该项目涉及与莫尔黑德天文馆的合作，该项目利用首席研究员在非正式教育方面的丰富经验，通过卡罗莱纳科学咖啡馆S促进公众对话。此外，来自代表性不足群体的本科生将在整个项目期间接受指导，进行研究。最后，这项研究的结果将有助于开发微型飞行器在复杂环境中导航。该方案的目标是揭示苍蝇在控制灯笼从而控制它们的空中动作时所使用的感觉编码和感觉运动处理的原理。这项研究将专注于果蝇，并将新的体内成像技术与来自计算神经科学和肌肉电生理学的分析方法相结合。通过表达基因编码的光学钙传感器GCaMP，可以直接观察到视觉制导飞行动作中笼形感受器的活动。这些实验将检验这一假设，即吊灯的特定区域编码视觉运动的不同方面，如方向或角速度。然后，将使用反向相关分析来构建量化模型，以测试在主动动作期间这些不同区域是以线性方式还是以非线性方式被招募。最后，如果翼部肌肉的功能分区是从缰骨的特定区域产生的，那么同时进行的机翼操纵肌的钙成像和电生理学将解决这一问题。此外，这项工作将演示机械传感器的布置和位置如何作为行为相关刺激的过滤器。通过采用有机方法，并将感官结构的微观机制与飞行行为联系起来，这些实验将清楚地说明导致吊灯进化的选择压力。这一奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

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.