Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Visual place learning in Drosophila melanogaster

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.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Drosophila trained in a thermal–visual arena show place learning.
Figure 2: Flies use visual cues to improve in place learning tasks.
Figure 3: Trained flies show a persistent search bias in the absence of the cool tile and retain this memory for several hours.
Figure 4: Subsets of ellipsoid body ring neurons are required for place learning.

References

  1. 1

    Mizunami, M., Weibrecht, J. M. & Strausfeld, N. J. Mushroom bodies of the cockroach: their participation in place memory. J. Comp. Neurol. 402, 520–537 (1998)

    CAS  Article  Google Scholar 

  2. 2

    Wessnitzer, J., Mangan, M. & Webb, B. Place memory in crickets. Proc. R. Soc. B 275, 915–921 (2008)

    Article  Google Scholar 

  3. 3

    Wehner, R. & Raber, F. Visual spatial memory in desert ants, Cataglyphis bicolor (Hymenoptera: Formicidae). Experientia 35, 1569–1571 (1979)

    Article  Google Scholar 

  4. 4

    Cartwright, B. A. & Collett, T. S. How honey bees use landmarks to guide their return to a food source. Nature 295, 560–564 (1982)

    ADS  Article  Google Scholar 

  5. 5

    Ernst, R. & Heisenberg, M. The memory template in Drosophila pattern vision at the flight simulator. Vision Res. 39, 3920–3933 (1999)

    CAS  Article  Google Scholar 

  6. 6

    Tang, S. & Guo, A. Choice behavior of Drosophila facing contradictory visual cues. Science 294, 1543–1547 (2001)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Capaldi, E. A. & Dyer, F. C. The role of orientation flights on homing performance in honeybees. J. Exp. Biol. 202, 1655–1666 (1999)

    CAS  PubMed  Google Scholar 

  8. 8

    Moser, E. I., Kropff, E. & Moser, M. B. Place cells, grid cells, and the brain’s spatial representation system. Annu. Rev. Neurosci. 31, 69–89 (2008)

    CAS  Article  Google Scholar 

  9. 9

    Morris, R. G. M. Spatial localization does not require the presence of local cues. Learn. Motiv. 12, 239–260 (1981)

    Article  Google Scholar 

  10. 10

    Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T. & Bate, M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523–1531 (2001)

    CAS  Article  Google Scholar 

  11. 11

    McGuire, S. E., Mao, Z. & Davis, R. L. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila . Sci. STKE 2004, pl6 (2004)

    PubMed  Google Scholar 

  12. 12

    Waddell, S. & Quinn, W. G. What can we teach Drosophila? What can they teach us? Trends Genet. 17, 719–726 (2001)

    CAS  Article  Google Scholar 

  13. 13

    de Belle, J. S. & Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692–695 (1994)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Wolf, R. et al. Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learn. Mem. 5, 166–178 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Putz, G. & Heisenberg, M. Memories in Drosophila heat-box learning. Learn. Mem. 9, 349–359 (2002)

    Article  Google Scholar 

  16. 16

    Heisenberg, M. Mushroom body memoir: from maps to models. Nature Rev. Neurosci. 4, 266–275 (2003)

    CAS  Article  Google Scholar 

  17. 17

    Neuser, K., Triphan, T., Mronz, M., Poeck, B. & Strauss, R. Analysis of a spatial orientation memory in Drosophila . Nature 453, 1244–1247 (2008)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Strauss, R. The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12, 633–638 (2002)

    CAS  Article  Google Scholar 

  19. 19

    Bernstein, S. & Bernstein, R. A. Relationships between foraging efficiency and size of head and component brain and sensory structures in red wood ant. Brain Res. 16, 85–104 (1969)

    CAS  Article  Google Scholar 

  20. 20

    Fahrbach, S. E. & Robinson, G. E. Behavioral development in the honey bee: toward the study of learning under natural conditions. Learn. Mem. 2, 199–224 (1995)

    CAS  Article  Google Scholar 

  21. 21

    Stocker, R. F. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3–26 (1994)

    CAS  Article  Google Scholar 

  22. 22

    Tully, T. & Quinn, W. G. Classical conditioning and retention in normal and mutant Drosophila melanogaster . J. Comp. Physiol. A 157, 263–277 (1985)

    CAS  Article  Google Scholar 

  23. 23

    Wustmann, G., Rein, K., Wolf, R. & Heisenberg, M. A new paradigm for operant conditioning of Drosophila melanogaster . J. Comp. Physiol. A 179, 429–436 (1996)

    CAS  Article  Google Scholar 

  24. 24

    Zars, T. Spatial orientation in Drosophila . J. Neurogenet. 23, 104–110 (2009)

    Article  Google Scholar 

  25. 25

    Morris, R. G., Schenk, F., Tweedie, F. & Jarrard, L. E. Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur. J. Neurosci. 2, 1016–1028 (1990)

    Article  Google Scholar 

  26. 26

    Seelig, J. D. et al. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nature Methods 7, 535–540 (2010)

    CAS  Article  Google Scholar 

  27. 27

    Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L. & Tank, D. W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nature Neurosci. 13, 1433–1440 (2010)

    CAS  Article  Google Scholar 

  28. 28

    Foucaud, J., Burns, J. G. & Mery, F. Use of spatial information and search strategies in a water maze analog in Drosophila melanogaster. PLoS ONE 5, e15231 (2010)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Reiser, M. B. & Dickinson, M. H. A modular display system for insect behavioral neuroscience. J. Neurosci. Methods 167, 127–139 (2008)

    Article  Google Scholar 

  30. 30

    Branson, K., Robie, A. A., Bender, J., Perona, P. & Dickinson, M. H. High-throughput ethomics in large groups of Drosophila. Nature Methods 6, 451–457 (2009)

    CAS  Article  Google Scholar 

  31. 31

    Sayeed, O. & Benzer, S. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl Acad. Sci. USA 93, 6079–6084 (1996)

    ADS  CAS  Article  Google Scholar 

  32. 32

    Zars, T. Two thermosensors in Drosophila have different behavioral functions. J. Comp. Physiol. A 187, 235–242 (2001)

    CAS  Article  Google Scholar 

  33. 33

    Strauss, R., Schuster, S. & Gotz, K. G. Processing of artificial visual feedback in the walking fruit fly Drosophila melanogaster. J. Exp. Biol. 200, 1281–1296 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Wustmann, G. & Heisenberg, M. Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. Learn. Mem. 4, 328–336 (1997)

    CAS  Article  Google Scholar 

  35. 35

    Zars, T., Wolf, R., Davis, R. & Heisenberg, M. Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. Learn. Mem. 7, 18–31 (2000)

    CAS  Article  Google Scholar 

  36. 36

    Diegelmann, S., Zars, M. & Zars, T. Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila. Learn. Mem. 13, 72–83 (2006)

    Article  Google Scholar 

  37. 37

    Dickinson, M. H. Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster. Phil. Trans R. Soc. B 354, 903–916 (1999)

    CAS  Article  Google Scholar 

  38. 38

    de Belle, J. S. & Heisenberg, M. Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc. Natl Acad. Sci. USA 93, 9875–9880 (1996)

    ADS  CAS  Article  Google Scholar 

  39. 39

    Pfeiffer, B. D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl Acad. Sci. USA 105, 9715–9720 (2008)

    ADS  CAS  Article  Google Scholar 

  40. 40

    Martin, J. R., Raabe, T. & Heisenberg, M. Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J. Comp. Physiol. A 185, 277–288 (1999)

    CAS  Article  Google Scholar 

Download references

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

Authors

Contributions

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

Corresponding authors

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

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-8 with legends and Supplementary Movie legends. (PDF 5727 kb)

Supplementary Movie 1

The movie shows a typical trial of place learning in the thermal visual arena (see Supplementary Information file for full legend). (MOV 10627 kb)

Supplementary Movie 2

The movie shows a typical probe trial following training with a coupled visual panorama (see Supplementary Information file for full legend). (MOV 3707 kb)

Supplementary Movie 3

This movie shows a typical probe trail following training with an uncoupled visual panorama (see Supplementary Information file for full legend). (MOV 3414 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ofstad, T., Zuker, C. & Reiser, M. Visual place learning in Drosophila melanogaster. Nature 474, 204–207 (2011). https://doi.org/10.1038/nature10131

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing