Diverse food-sensing neurons trigger idiothetic local search in Drosophila
Foraging animals may benefit from remembering the location of a newly discovered food patch while continuing to explore nearby [1, 2]. For example, after encountering a drop of yeast or sugar, hungry flies often perform a local search [3, 4]. That is, rather than remaining on the food or simply walking away, flies execute a series of exploratory excursions during which they repeatedly depart and return to the resource. Fruit flies, Drosophila melanogaster, can perform this food-centered search behavior in the absence of external landmarks, instead relying on internal (idiothetic) cues . This path-integration behavior may represent a deeply conserved navigational capacity in insects [6, 7], but its underlying neural basis remains unknown. Here, we used optogenetic activation to screen candidate cell classes and found that local searches can be initiated by diverse sensory neurons. Optogenetically induced searches resemble those triggered by actual food, are modulated by starvation state, and exhibit key features of path integration. Flies perform tightly centered searches around the fictive food site, even within a constrained maze, and they can return to the fictive food site after long excursions. Together, these results suggest that flies enact local searches in response to a wide variety of food-associated cues and that these sensory pathways may converge upon a common neural system for navigation. Using a virtual reality system, we demonstrate that local searches can be optogenetically induced in tethered flies walking on a spherical treadmill, laying the groundwork for future studies to image the brain during path integration.
© 2019 Elsevier Ltd. Received 10 October 2018, Revised 21 January 2019, Accepted 6 March 2019, Available online 2 May 2019. We wish to thank Francesca V. Ponce for helpful discussions and assistance with preparing the synthetic food medium. Rubi Salgado assisted with fly rearing. Annie Rak helped with conducting the PER experiments. Ysabel M. Giraldo and Katherine J. Leitch provided advice on statistical analysis. Floris van Breugel and Theodore H. Lindsay helped implement the software used for tracking and closed-loop optogenetic stimulation. William B. Dickson created the software for closed-loop virtual fictive food sites, fabricated the balls for the spherical treadmill, and assisted in data analysis. Kristin Scott and John Carlson kindly provided us with flies. Research reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award U19NS104655. Author Contributions: R.A.C. conducted all experiments, except those in Figure 4, which were performed by T.S. R.A.C. analyzed all data and prepared all figures. R.A.C. and M.H.D. conceived of experiments and wrote the paper. The authors declare no competing interests.
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