Letter

Visual place learning in Drosophila melanogaster

Received:
Accepted:
Published online:

Abstract

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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Acknowledgements

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.

Author information

Affiliations

  1. Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA

    • Tyler A. Ofstad
    • , Charles S. Zuker
    •  & Michael B. Reiser
  2. Department of Neurosciences, Howard Hughes Medical Institute, University of California at San Diego, La Jolla, California 92093-0649, USA

    • Tyler A. Ofstad
    •  & Charles S. Zuker
  3. Department of Neurobiology, Howard Hughes Medical Institute, University of California at San Diego, La Jolla, California 92093-0649, USA

    • Charles S. Zuker
  4. Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA

    • Charles S. Zuker
  5. Department of Neuroscience, Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA

    • Charles S. Zuker

Authors

  1. Search for Tyler A. Ofstad in:

  2. Search for Charles S. Zuker in:

  3. Search for Michael B. Reiser in:

Contributions

All authors designed the study and wrote the manuscript. T.A.O. carried out the experiments and data analysis.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Charles S. Zuker or Michael B. Reiser.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    The file contains Supplementary Figures 1-8 with legends and Supplementary Movie legends.

Videos

  1. 1.

    Supplementary Movie 1

    The movie shows a typical trial of place learning in the thermal visual arena (see Supplementary Information file for full legend).

  2. 2.

    Supplementary Movie 2

    The movie shows a typical probe trial following training with a coupled visual panorama (see Supplementary Information file for full legend).

  3. 3.

    Supplementary Movie 3

    This movie shows a typical probe trail following training with an uncoupled visual panorama (see Supplementary Information file for full legend).

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