Asynchronous haltere input drives specific wing and head movements in Drosophila.

Halteres are multifunctional mechanosensory organs unique to the true flies (Diptera). A set of reduced hindwings, the halteres beat at the same frequency as the lift-generating forewings and sense inertial forces via mechanosensory campaniform sensilla. Though haltere ablation makes stable flight impossible, the specific role of wing-synchronous input has not been established. Using small iron filings attached to the halteres of tethered flies and an alternating electromagnetic field, we experimentally decoupled the wings and halteres of flying Drosophila and observed the resulting changes in wingbeat amplitude and head orientation. We find that asynchronous haltere input results in fast amplitude changes in the wing (hitches), but does not appreciably move the head. In multi-modal experiments, we find that wing and gaze optomotor responses are disrupted differently by asynchronous input. These effects of wing-asynchronous haltere input suggest that specific sensory information is necessary for maintaining wing amplitude stability and adaptive gaze control.

Haltere and visual inputs sum linearly to predict wing (but not gaze) motor output in tethered flying Drosophila.

In the true flies (Diptera), the hind wings have evolved into specialized mechanosensory organs known as halteres, which are sensitive to gyroscopic and other inertial forces. Together with the fly's visual system, the halteres direct head and wing movements through a suite of equilibrium reflexes that are crucial to the fly's ability to maintain stable flight. As in other animals (including humans), this presents challenges to the nervous system as equilibrium reflexes driven by the inertial sensory system must be integrated with those driven by the visual system in order to control an overlapping pool of motor outputs shared between the two of them. Here, we introduce an experimental paradigm for reproducibly altering haltere stroke kinematics and use it to quantify multisensory integration of wing and gaze equilibrium reflexes. We show that multisensory wing-steering responses reflect a linear superposition of haltere-driven and visually driven responses, but that multisensory gaze responses are not well predicted by this framework. These models, based on populations, extend also to the responses of individual flies.

Inertial Sensing and Encoding of Self-Motion: Structural and Functional Similarities across Metazoan Taxa.

To properly orient and navigate, moving animals must obtain information about the position and motion of their bodies. Animals detect inertial signals resulting from body accelerations and rotations using a variety of sensory systems. In this review, we briefly summarize current knowledge on inertial sensing across widely disparate animal taxa with an emphasis on neuronal coding and sensory transduction. We outline systems built around mechanosensory hair cells, including the chordate vestibular complex and the statocysts seen in many marine invertebrates. We next compare these to schemes employed by flying insects for managing inherently unstable aspects of flapping flight, built around comparable mechanosensory cells but taking unique advantage of the physics of rotating systems to facilitate motion encoding. Finally, we highlight fundamental similarities across taxa with respect to the partnering of inertial senses with visual senses and conclude with a discussion of the functional utility of maintaining a multiplicity of encoding schemes for self-motion information.