Antennal Mechanosensory Neurons Mediate Wing Motor Reflexes in Flying Drosophila
Although many behavioral studies have shown the importance of antennal mechanosensation in various aspects of insect flight control, the identities of the mechanosensory neurons responsible for these functions are still unknown. One candidate is the Johnston's organ (JO) neurons that are located in the second antennal segment and detect phasic and tonic rotations of the third antennal segment relative to the second segment. To investigate how different classes of JO neurons respond to different types of antennal movement during flight, we combined 2-photon calcium imaging with a machine vision system to simultaneously record JO neuron activity and the antennal movement from tethered flying fruit flies (Drosophila melanogaster). We found that most classes of JO neurons respond strongly to antennal oscillation at the wing beat frequency, but not to the tonic deflections of the antennae. To study how flies use input from the JO neurons during flight, we genetically ablated specific classes of JO neurons and examined their effect on the wing motion. Tethered flies flying in the dark require JO neurons to generate slow antiphasic oscillation of the left and right wing stroke amplitudes. However, JO neurons are not necessary for this antiphasic oscillation when visual feedback is available, indicating that there are multiple pathways for generating antiphasic movement of the wings. Collectively, our results are consistent with a model in which flying flies use JO neurons to detect increases in the wing-induced airflow and that JO neurons are involved in a response that decreases contralateral wing stoke amplitude.
© 2015 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. 5, 2015; revised April 8, 2015; accepted April 13, 2015. This work was supported by the Paul G. Allen Family Foundation to M.H.D. We thank Allan Wong for flies (JO1, JO-AB, JO-CE, and F GAL4 drivers, and JO-CE;eyeflp flies); Anne Sustar and Ainul Huda for technical assistance; and Bettina Schnell, Marie P. Suver, and Peter T. Weir for helpful discussions and comments. Author contributions: A.M. and M.H.D. designed research; A.M. performed research; A.M. analyzed data; A.M. and M.H.D. wrote the paper.
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