The ability of insects to learn and navigate to specific locations in the environment has fascinated naturalists for decades. The impressive navigational abilities of ants, bees, wasps and other insects demonstrate that insects are capable of visual place learning1,2,3,4, but little is known about the underlying neural circuits that mediate these behaviours. Drosophila melanogaster (common fruit fly) is a powerful model organism for dissecting the neural circuitry underlying complex behaviours, from sensory perception to learning and memory. Drosophila can identify and remember visual features such as size, colour and contour orientation5,6. However, the extent to which they use vision to recall specific locations remains unclear. Here we describe a visual place learning platform and demonstrate that Drosophila are capable of forming and retaining visual place memories to guide selective navigation. By targeted genetic silencing of small subsets of cells in the Drosophila brain, we show that neurons in the ellipsoid body, but not in the mushroom bodies, are necessary for visual place learning. Together, these studies reveal distinct neuroanatomical substrates for spatial versus non-spatial learning, and establish Drosophila as a powerful model for the study of spatial memories.
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We particularly thank M. Gallio for help with thermosensation and the development of temperature behavioural tests. We also thank G. Rubin for providing GAL4 lines before publication, A. Jenett for their anatomical annotation and M. Dickinson for discussions and advice. Brain images were provided by the Janelia Fly Light Project. T. Laverty and the Janelia Fly Core assisted with Drosophila maintenance. Additional support was provided by J. Osborne, C. Werner, D. Olbris and M. Bolstad. We also thank V. Jayaraman, members of the Reiser and Zuker labs, Janelia Farm colleagues and the Janelia Fly Olympiad Project. This project was supported through the HHMI Janelia Farm Research Campus visitor programmed (T.A.O. and C.S.Z., hosted by M.B.R.). C.S.Z. is a HHMI investigator and a Senior Fellow at Janelia Farm.
The movie shows a typical trial of place learning in the thermal visual arena (see Supplementary Information file for full legend).
The movie shows a typical probe trial following training with a coupled visual panorama (see Supplementary Information file for full legend).
This movie shows a typical probe trail following training with an uncoupled visual panorama (see Supplementary Information file for full legend).
About this article
Nature Neuroscience (2017)