Functional Stratification of Sensory Encoding in a Biological Gyroscope
From May 2022 to May 2024
Abstract
As a postdoc in Bradley Dickerson's lab at Princeton Neuroscience Institute, I worked on the neurobiology of a specific Dipteran species linked to a strong genetic toolkit, the fruit fly Drosophila melanogaster. Flies have developed elegant solutions to navigate their environment. One of the reasons for Dipterans’ flight abilities comes from the halteres, a specialized mechanosensory organ known to be the only biological gyroscope. Recent work shows that the haltere also provides crucial timing information to the flight circuit on a stroke-by-stroke basis via modulation of a set of tiny muscles that are inserted at the base of the haltere. This sensory input helps structure the timing of the steering muscles, which ultimately control wing motion and aerodynamic force production. Halteres are covered in arrays of strain-sensitive mechanosensors known as campaniform sensilla, that are arranged in distinct groups on the dorsal and ventral aspects of the haltere and may exhibit different directional sensitivities. However, due to the difficulty of studying the haltere–a tiny moving structure–during flight, this longstanding hypothesis remains untested. Using a genetically encoded calcium indicator expressed in the haltere afferents of Drosophila, my goal was to uncover how sensory information is encoded by these arrays during visually mediated flight manoeuvres.
I developed an experimental setup to record the activity changes in the dorsal haltere campaniforms during tethered flight while presenting flies with an array of visual motion stimuli. To do this, I imaged through the cuticle of the haltere with a standard epifluorescent microscope, all while leaving the animal intact. I found that during wide-field visual motion, haltere campaniform sensilla activity is modulated throughout the flight. Additionally, during spontaneous turning events termed saccades, each dorsal field is recruited prior to the turning event. This result suggests that, in addition to their previously known role in terminating active turns, halteres are implicated in triggering saccades. Finally, saccade amplitude appears to be correlated with the level of campaniform field recruitment. Specifically, this relationship appears to be nonlinear as larger changes in ipsilateral wingstroke amplitude are correlated with increases in campaniform field fluorescence. In conclusion, these results support the hypothesis that the haltere steering muscles of Drosophila receive descending visual input, suggesting that flies, through the halteres, may tune the strength of haltere mechanosensory feedback to achieve flight turns. My results demonstrate the crucial role of biomechanics in determining the dynamic range of sensors so that they can mediate manoeuvres for both stabilization and active manoeuvres.
In the meantime, I worked on the ascending connectivity between the haltere and neck. It has been postulated that gaze stabilization, essential to stable flight, is facilitated by ascending mechanosensory information from the haltere We however lack evidence for such a circuit. To bridge this gap in our understanding, I used electron microscopy connectomics to map the synaptic connectivity between the haltere sensory afferents and those motor neurons responsible for head steering movements. In parallel, I developed custom machine vision software to quantify 3-dimensional head movements in tethered flies and will implement it in my previous rig to correlate haltere activity with gaze.
