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.

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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.

References

  1. 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. 2

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

    CAS  Article  Google Scholar 

  3. 3

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

    ADS  CAS  Article  Google Scholar 

  4. 4

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

    ADS  CAS  Article  Google Scholar 

  5. 5

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

    CAS  Article  Google Scholar 

  6. 6

    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 

  7. 7

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

    ADS  CAS  Article  Google Scholar 

  8. 8

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

    CAS  Article  Google Scholar 

  9. 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. 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)

    ADS  CAS  Article  Google Scholar 

  11. 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)

    CAS  Article  Google Scholar 

  12. 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)

    CAS  Article  Google Scholar 

  13. 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)

    CAS  Article  Google Scholar 

  14. 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)

    CAS  Article  Google Scholar 

  15. 15

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

    ADS  CAS  Article  Google Scholar 

  16. 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)

    ADS  CAS  Article  Google Scholar 

  17. 17

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

    ADS  CAS  Article  Google Scholar 

  18. 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)

    ADS  CAS  Article  Google Scholar 

  19. 19

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

    CAS  Article  Google Scholar 

  20. 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)

    CAS  Article  Google Scholar 

  21. 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. 22

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

    CAS  Article  Google Scholar 

  23. 23

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

    ADS  CAS  Article  Google Scholar 

  24. 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. 25

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

    Google Scholar 

  26. 26

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

    CAS  Article  Google Scholar 

  27. 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)

    CAS  Article  Google Scholar 

  28. 28

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

    CAS  Article  Google Scholar 

  29. 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. 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)

    CAS  Article  Google Scholar 

  31. 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)

    CAS  Article  Google Scholar 

  32. 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. 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. 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. 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)

    CAS  Article  Google Scholar 

  36. 36

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

    CAS  Article  Google Scholar 

  37. 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.).

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Correspondence to Li Liu.

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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)

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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

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