Active and Passive Antennal Movements during Visually Guided Steering in Flying Drosophila
Insects use feedback from a variety of sensory modalities, including mechanoreceptors on their antennae, to stabilize the direction and speed of flight. Like all arthropod appendages, antennae not only supply sensory information but may also be actively positioned by control muscles. However, how flying insects move their antennae during active turns and how such movements might influence steering responses are currently unknown. Here we examined the antennal movements of flying Drosophila during visually induced turns in a tethered flight arena. In response to both rotational and translational patterns of visual motion, Drosophila actively moved their antennae in a direction opposite to that of the visual motion. We also observed two types of passive antennal movements: small tonic deflections of the antenna and rapid oscillations at wing beat frequency. These passive movements are likely the result of wing-induced airflow and increased in magnitude when the angular distance between the wing and the antenna decreased. In response to rotational visual motion, increases in passive antennal movements appear to trigger a reflex that reduces the stroke amplitude of the contralateral wing, thereby enhancing the visually induced turn. Although the active antennal movements significantly increased antennal oscillation by bringing the arista closer to the wings, it did not significantly affect the turning response in our head-fixed, tethered flies. These results are consistent with the hypothesis that flying Drosophila use mechanosensory feedback to detect changes in the wing induced airflow during visually induced turns and that this feedback plays a role in regulating the magnitude of steering responses.
© 2011 The Authors. For the first six months after publication SfN's license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN's website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received Jan. 28, 2011; revised March 10, 2011; accepted March 17, 2011. This work was supported by National Science Foundation Frontiers in Integrative Biological Research Award 0623527 (M.H.D.). We thank Martin Peek for technical assistance and Gaby Maimon for helpful discussion and comments. Author contributions: A.M., A.D.S., and M.H.D. designed research; A.M. performed research; A.D.S. and E.T. contributed unpublished reagents/analytic tools; A.M. analyzed data; A.M. and M.H.D. wrote the paper.
Published - Mamiya2011p13904J_Neurosci.pdf