Sun Navigation Requires Compass Neurons in Drosophila

• Published in: Current biology 2018-09, Vol.28 (17), p.2845-2852.e4
• Main Authors: Giraldo, Ysabel Milton, Leitch, Katherine J., Ros, Ivo G., Warren, Timothy L., Weir, Peter T., Dickinson, Michael H.
• Format: Article
• Language: English
• Subjects: Animals; Brain - physiology; central complex; Cues; Drosophila melanogaster - physiology; navigation; Neurons - physiology; Orientation - physiology; Orientation, Spatial - physiology; sun compass; Sunlight
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2018.07.002

Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2–9], 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 [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], 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 [17–19], similar to mammalian head-direction cells [20]. 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. •Flying Drosophila can navigate a straight path using the position of the sun•Flies can remember their sun compass heading from one flight to the next•Sun position is encoded by compass cells within the central complex of the brain•Genetic silencing of compass cells within the brain interferes with sun navigation Giraldo et al. find that flying Drosophila navigate by holding the sun at a fixed position, which they remember across successive flights. Imaging experiments reveal a class of neurons in the brain that track the motion of the sun. When these cells are silenced, flies no longer adopt and maintain arbitrary headings but instead exhibit phototaxis.