Neural evidence supports a dual sensory-motor role for insect wings

Abstract

Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low light conditions. While halteres in dipteran species are well known to provide such information for flight control, less is understood about the mechanosensory roles of their evolutionary antecedent, wings. The features that wing mechanosensory neurons (campaniform sensilla) encode remains relatively unexplored. We hypothesized that the wing campaniform sensilla of the hawkmoth, Manduca sexta, rapidly and selectively extract mechanical stimulus features in a manner similar to halteres. We used electrophysiological and computational techniques to characterize the encoding properties of wing campaniform sensilla. To accomplish this, we developed a novel technique for localizing receptive fields using a focused IR laser that elicits changes in the neural activity of mechanoreceptors. We found that (i) most wing mechanosensors encoded mechanical stimulus features rapidly and precisely, (ii) they are selective for specific stimulus features, and (iii) there is diversity in the encoding properties of wing campaniform sensilla. We found that the encoding properties of wing campaniform sensilla are similar to those for haltere neurons. Therefore, it appears that the neural architecture that underlies the haltere sensory function is present in wings, which lends credence to the notion that wings themselves may serve a similar sensory function. Thus, wings may not only function as the primary actuator of the organism but also as sensors of the inertial dynamics of the animal.