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.

  • Article
  • Published:

Distinct memory traces for two visual features in the Drosophila brain

Abstract

The fly Drosophila melanogaster can discriminate and remember visual landmarks. It analyses selected parts of its visual environment according to a small number of pattern parameters such as size, colour or contour orientation, and stores particular parameter values. Like humans, flies recognize patterns independently of the retinal position during acquisition of the pattern (translation invariance). Here we show that the central-most part of the fly brain, the fan-shaped body, contains parts of a network mediating visual pattern recognition. We have identified short-term memory traces of two pattern parameters—elevation in the panorama and contour orientation. These can be localized to two groups of neurons extending branches as parallel, horizontal strata in the fan-shaped body. The central location of this memory store is well suited to mediate translational invariance.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Flight simulator for measuring visual pattern recognition.
Figure 2: Visual pattern memory is impaired in central complex mutants.
Figure 3: Expression patterns of three driver lines rescuing pattern memory.
Figure 4: Rescue and suppression of pattern memory occur in the adult.
Figure 5: Memory traces for pattern parameters are spatially separated.

Similar content being viewed by others

References

  1. Heisenberg, M. & Wolf, R. On the fine structure of yaw torque in visual flight orientation of Drosophila melanogaster. J. Comp. Physiol. [A] 130, 113–130 (1979)

    Article  Google Scholar 

  2. Xia, S., Liu, L., Feng, C. & Guo, A. Memory consolidation in Drosophila operant visual learning. Learn. Mem. 4, 205–218 (1997)

    Article  CAS  Google Scholar 

  3. Dill, M. & Heisenberg, M. Visual pattern memory without shape recognition. Phil. Trans. R. Soc. Lond. B 349, 143–152 (1995)

    Article  ADS  CAS  Google Scholar 

  4. Dill, M., Wolf, R. & Heisenberg, M. Visual pattern recognition in Drosophila involves retinotopic matching. Nature 365, 751–753 (1993)

    Article  ADS  CAS  Google Scholar 

  5. Dill, M., Wolf, R. & Heisenberg, M. Behavioral analysis of Drosophila landmark learning in the flight simulator. Learn. Mem. 2, 152–160 (1995)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Tang, S., Wolf, R., Xu, S. & Heisenberg, M. Visual pattern recognition in Drosophila is invariant for retinal position. Science 305, 1020–1022 (2004)

    Article  ADS  CAS  Google Scholar 

  8. Gerber, B., Tanimoto, H. & Heisenberg, M. An engram found? Evaluating the evidence from fruit flies. Curr. Opin. Neurobiol. 14, 737–744 (2004)

    Article  CAS  Google Scholar 

  9. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993)

    CAS  Google Scholar 

  10. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. & Davis, R. L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765–1768 (2003)

    Article  ADS  CAS  Google Scholar 

  11. Dudai, Y., Corfas, G. & Hazvi, S. What is the possible contribution of Ca2+-stimulated adenylate cyclase to acquisition, consolidation and retention of an associative olfactory memory in Drosophila. J. Comp. Physiol. [A] 162, 101–109 (1988)

    Article  CAS  Google Scholar 

  12. Levin, L. R. et al. The Drosophila learning and memory gene rutabaga encodes a Ca2+/Calmodulin-responsive adenylyl cyclase. Cell 68, 479–489 (1992)

    Article  CAS  Google Scholar 

  13. Abrams, T. W., Yovell, Y., Onyike, C. U., Cohen, J. E. & Jarrard, H. E. Analysis of sequence-dependent interactions between transient calcium and transmitter stimuli in activating adenylyl cyclase in Aplysia: possible contribution to CS–US sequence requirement during conditioning. Learn. Mem. 4, 496–509 (1998)

    Article  CAS  Google Scholar 

  14. Renger, J. J., Ueda, A., Atwood, H. L., Govind, C. K. & Wu, C. F. Role of cAMP cascade in synaptic stability and plasticity: ultrastructural and physiological analyses of individual synaptic boutons in Drosophila memory mutants. J. Neurosci. 20, 3980–3992 (2000)

    Article  CAS  Google Scholar 

  15. Zars, T., Fischer, M., Schulz, R. & Heisenberg, M. Localization of a short-term memory in Drosophila. Science 288, 672–675 (2000)

    Article  ADS  CAS  Google Scholar 

  16. McGuire, S. E., Le, P. T. & Davis, R. L. The role of Drosophila mushroom body signalling in olfactory memory. Science 293, 1330–1333 (2001)

    Article  ADS  CAS  Google Scholar 

  17. Connolly, J. B. et al. Associative learning disrupted by impaired Gs signalling in Drosophila mushroom bodies. Science 274, 2104–2107 (1996)

    Article  ADS  CAS  Google Scholar 

  18. Dubnau, J., Grady, L., Kitamoto, T. & Tully, T. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411, 476–480 (2001)

    Article  ADS  CAS  Google Scholar 

  19. Schwaerzel, M., Heisenberg, M. & Zars, T. Extinction antagonizes olfactory memory at the subcellular level. Neuron 35, 951–960 (2002)

    Article  CAS  Google Scholar 

  20. 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)

    Article  CAS  Google Scholar 

  21. Heisenberg, M. Central Brain Function in Insects: Genetic Studies on the Mushroom Bodies and Central Complex in Drosophila (eds Schildberger, K. & Elsner, N.) (Gustav Fischer, Stuttgart/Jena/New York, 1994)

    Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Homberg, U. In search of the sky compass in the insect brain. Naturwissenschaften 91, 199–208 (2004)

    Article  ADS  CAS  Google Scholar 

  24. Strauss, R. Die übergeordnete Steuerung des Laufverhaltens durch das Insektengehirn, studiert mit Methoden der Drosophila-Neurogenetik. Habilitation thesis, Bayerische Julius-Maximilians-Universität, Wuerzburg (2002)

    Google Scholar 

  25. Weidtmann, N. Visuelle Flugsteuerung und Verhaltensplastizität bei Zentralkomplexmutanten von Drosophila melanogaster. Diploma thesis, Bayerische Julius-Maximilians-Universität, Wuerzburg (1993)

    Google Scholar 

  26. Strauss, R. & Heisenberg, M. A higher control center of locomotor behaviour in the Drosophila brain. J. Neurosci. 13, 1852–1861 (1993)

    Article  CAS  Google Scholar 

  27. Keller, A., Sweeney, S. T., Zars, T., O'Kane, C. J. & Heisenberg, M. Targeted expression of tetanus neurotoxin interferes with behavioural responses to sensory input in Drosophila. J. Neurobiol. 50, 221–233 (2002)

    Article  CAS  Google Scholar 

  28. Broadie, K. et al. Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15, 663–673 (1995)

    Article  CAS  Google Scholar 

  29. Eyding, D. Lernen und Kurzzeitgedächtnis beim operanten Konditionieren auf visuelle Muster bei strukturellen und biochemischen Mutanten von Drosophila melanogaster. Diploma thesis, Bayerische Julius-Maximilians-Universität, Wuerzburg (1993)

    Google Scholar 

  30. Brembs, B. & Heisenberg, M. The operant and the classical in conditioned orientation of Drosophila melanogaster at the flight simulator. Learn. Mem. 7, 104–115 (2000)

    Article  CAS  Google Scholar 

  31. Prokop, A. & Technau, G. M. Normal function of the mushroom body defect gene of Drosophila is required for the regulation of the number and proliferation of neuroblasts. Dev. Biol. 161, 321–337 (1994)

    Article  CAS  Google Scholar 

  32. 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 

  33. Fischbach, K. F. & Dittrich, A. P. M. The optic lobe of Drosophila melanogaster. A Golgi analysis of wild-type structure. Cell Tissue Res. 258, 441–475 (1989)

    Article  Google Scholar 

  34. Hanesch, U., Fischbach, K. F. & Heisenberg, M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257, 343–366 (1989)

    Article  Google Scholar 

  35. Vitzthum, H., Muller, M. & Homberg, U. Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J. Neurosci. 22, 1114–1125 (2002)

    Article  CAS  Google Scholar 

  36. Wolf, R. & Heisenberg, M. Basic organization of operant behaviour as revealed in Drosophila flight orientation. J. Comp. Physiol. [A] 169, 699–705 (1991)

    Article  CAS  Google Scholar 

  37. Heisenberg, M. & Wolf, R. Reafferent control of optomotor yaw torque in Drosophila melanogaster. J. Comp. Physiol. [A] 163, 373–388 (1988)

    Article  Google Scholar 

Download references

Acknowledgements

We thank B. Gerber and H. Tanimoto for valuable comments on the manuscript, C. Grübel, Haiyun Gong and Huoqing Jiang for excellent technical assistance, and A. Jenett for visualizing gene expression patterns. Supported by Deutsche Forschungsgemeinschaft, Fonds der Chemischen Industrie (M.H.), National Natural Sciences Foundation of China (L.L.), ‘973-program’ (L.L.), and by the Knowledge Innovation Project of the Chinese Academy of Sciences (L.L.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Li Liu.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Figures 1–3, Supplementary Tables 1 and 2, Supplementary Methods and Supplementary Discussion. The Supplementary Figures show the dynamics of flight orientation behaviour of a single fly (raw data) during a learning experiment in the flight simulator (Supplementary Fig. 1), the expression patterns for all 7 driver lines which rescue the rut-dependent memory defect for pattern elevation (Supplementary Fig. 2), and a 3-D reconstruction of the tangential layer-5 Neurons (F5) in the fan-shaped body (Supplementary Fig. 3). Supplementary Table 1 addresses pattern discrimination ability of fly lines which are deficient in pattern memory and Supplementary Table 2 contains a compilation of the results of all 28 rutabaga rescue experiments accomplished in this study. (PDF 572 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, G., Seiler, H., Wen, A. et al. Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551–556 (2006). https://doi.org/10.1038/nature04381

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04381

This article is cited by

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