An Array of Descending Visual Interneurons Encoding Self-Motion in Drosophila
The means by which brains transform sensory information into coherent motor actions is poorly understood. In flies, a relatively small set of descending interneurons are responsible for conveying sensory information and higher-order commands from the brain to motor circuits in the ventral nerve cord. Here, we describe three pairs of genetically identified descending interneurons that integrate information from wide-field visual interneurons and project directly to motor centers controlling flight behavior. We measured the physiological responses of these three cells during flight and found that they respond maximally to visual movement corresponding to rotation around three distinct body axes. After characterizing the tuning properties of an array of nine putative upstream visual interneurons, we show that simple linear combinations of their outputs can predict the responses of the three descending cells. Last, we developed a machine vision-tracking system that allows us to monitor multiple motor systems simultaneously and found that each visual descending interneuron class is correlated with a discrete set of motor programs.
© 2016 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 July 13, 2016; revised Sept. 22, 2016; accepted Sept. 24, 2016. This work was supported by the National Institute of Neurological Disorders and Stroke–National Institutes of Health (Grant U01NS090514 to M.H.D.) and the Paul G. Allen Family Foundation (M.H.D.). We thank Anne Sustar for assistance with fly stocks; Allan Wong for guidance with the photoactivatible GFP technique; Gwyneth Card and Shigehiro Namiki for useful discussions about the descending interneurons; and Katherine Nagel and Peter Weir for helpful comments on the manuscript. Author contributions: M.P.S. and M.H.D. designed research; M.P.S., A.H., and N.I. performed research; S.S. contributed unpublished reagents/analytic tools; M.P.S. analyzed data; M.P.S. and M.H.D. wrote the paper. The authors declare no competing financial interests.
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