The role of wing mechanosensory feedback in insect flight control
Dickerson, Bradley Horatio
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Flying insects rapidly stabilize after perturbations using multiple sensory modalities (e.g., vision mechanoreception, olfaction) for active control. Mechanoreceptors’ direct coupling of sensory structure to the environment, as opposed to the series of chemical cascades typical of photoreceptors, makes them critical components of locomotor control. For example, both dipteran (flies) and strepsipteran (twisted wing flies) insects possess pendular organs known as halteres that allow these animals to detect gyroscopic forces and correct for perturbations to the flight path. Yet, aside from the literature on halteres and recent work on the antennae of the hawkmoth Manduca sexta, it is unclear how other flying insects use mechanosensory information to control body dynamics. In Chapter 1, I review the role of sensory input in insect flight control, particularly mechanosensory information. Evolutionarily derived from the wings, halteres are essential to flight, providing information that allows flies to make rapid adjustments to their wing and body kinematics. During rotational maneuvers or instabilities during flight, halteres experience an inertial force that is orthogonal to the plane of oscillation, known as the Coriolis force. By definition, insect wings experience Coriolis forces during rotations. Further, the mechanosensory structures found on the halteres, campaniform sensilla, are also present on wings, suggesting that the wings can encode information about flight dynamics. In Chapter 2 (Dickerson et al., 2014), I test whether the wings can provide sensory information that helps informs the animal of its body dynamics. I use targeted manipulations of the wings to test for the presence of a reflex mediated by the embedded campaniform sensilla. I attach small rare-earth magnets to each wing and placed tethered moths within an electromagnet, thereby simulating an inertial stimulus around the animals’ pitch axis. This stimulus elicits the same abdominal flexion reflex these animals exhibit in response to visual or whole-body pitch stimuli of the same frequency and amplitude. These results demonstrate that the wings can provide information about body dynamics during locomotion, a role previously thought to be the sole domain of the halteres. In Chapter 3 (Eberle, Dickerson et al., 2015), I use computational and robotic models of a flapping, flexible wing subject to rotation to address whether the Coriolis force can be experimentally observed using only changes in the wing’s structural dynamics. I find that body rotation induces torsion that is the direct consequence of forces, including the Coriolis force, acting on the wings. I also find that this torsion changes the spatiotemporal pattern of strain across the wing. The emergent patterns of strain point to a mechanism by which flying insects could detect their angular velocity during perturbations or maneuvers via the structural dynamics of their wings. In Chapter 4, I extend the method developed to stimulate the wings in tethered flight to test how wing mechanosensory information interacts with the visual system. I subject moths to a moving sinusoidal grating in both dim and near-total darkness conditions, testing moths’ abdominal flexion response during visual stimulation alone and during simultaneous stimulation of the wings and visual system. I find no significant differences between the two groups at either light level, suggesting that moths will track a high contrast visual object, even in extremely dim conditions. My findings also support the wings’ role as context-dependent sensory structures.
- Biology