Sun Navigation Requires Compass Neurons in Drosophila
Despite their small brains, insects can navigate over long distances by orienting using visual landmarks , skylight polarization [2, 3, 4, 5, 6, 7, 8, 9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening . To accomplish such feats on available energy reserves , flies would have to maintain relatively straight headings, relying on celestial cues . Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway , including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17, 18, 19], similar to mammalian head-direction cells . Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights—even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior.
© 2018 Published by Elsevier Ltd. Received 6 June 2018, Revised 28 June 2018, Accepted 2 July 2018, Available online 30 August 2018. We thank Tanya Wolff and Gerry Rubin for generously providing us with the split-GAL4 lines SS00131 and SS00408 prior to the publication of their manuscript describing them. Crystal Liang and Aisling Murran provided valuable assistance with data collection. This work was funded by grants from the NSF (IOS 1547918), NIH (U19NS104655), and the Simons Foundation (71582123) to M.H.D., as well as an NIH NRSA postdoctoral fellowship (F32GM109777) to Y.M.G. Author Contributions: P.T.W. and T.L.W. were involved in early experimental design and collected preliminary data on sun orientation behavior. Y.M.G., K.J.L., I.G.R., and M.H.D. conceived of and conducted experiments. Y.M.G. characterized sun compass behavior (Figure 1), I.G.R. conducted functional imaging experiments (Figure 2), and Y.M.G. and K.J.L. performed genetic silencing experiments (Figure 3). Y.M.G., K.J.L., I.G.R., and M.H.D. wrote the paper. All authors contributed in editing the final manuscript. The authors declare no competing interests.
Supplemental Material - 1-s2.0-S0960982218309011-mmc1.pdf
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Accepted Version - nihms-1027095.pdf