A comparison of visual and haltere-mediated feedback in the control of body saccades in Drosophila melanogaster.
The flight trajectories of fruit flies consist of straight flight segments interspersed with rapid turns called body saccades. Although the saccades are stereotyped, it is not known whether their brief time course is due to a feed-forward (predetermined) motor program or due to feedback from sensory systems that are reflexively activated by the rapid rotation. Two sensory modalities, the visual system and the mechanosensory halteres, are likely sources of such feedback because they are sensitive to angular velocities within the range experienced during saccades. Utilizing a magnetic tether in which flies are fixed in space but free to rotate about their yaw axis, we systematically manipulated the feedback from the visual and haltere systems to test their role in determining the time course of body saccades. We found that altering visual feedback had no significant effect on the dynamics of saccades, whereas increasing and decreasing the amount of haltere-mediated feedback decreased and increased saccade amplitude, respectively. In other experiments, we altered the aerodynamic surface of the wings such that the flies had to actively modify their wing-stroke kinematics to maintain straight flight on the magnetic tether. Flies exhibit such modification, but the control is compromised in the dark, indicating that the visual system does provide feedback for flight stability at lower angular velocities, to which the haltere system is less sensitive. Cutting the wing surface disrupted the time course of the saccades, indicating that although flies employ sensory feedback to modulate saccade dynamics, it is not precise or fast enough to compensate for large changes in wing efficacy.
Bender
John A
JA
Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA. jbender@caltech.edu
Dickinson
Michael H
MH
D000818:Animals; D004331:Drosophila melanogaster / Q000502:physiology*; D005246:Feedback / Q000502:physiology; D005260:Female; D005426:Flight, Animal / Q000502:physiology*; D040542:Mechanotransduction, Cellular / Q000502:physiology*; D014785:Vision, Ocular / Q000502:physiology*; D014921:Wings, Animal / Q000033:anatomy & histology / Q000502:physiology*