Skip to main content

Active Vision in Blowflies: Strategies and Mechanisms of Spatial Orientation

  • Chapter
  • First Online:
Flying Insects and Robots

Abstract

With its miniature brain blowflies are able to control highly aerobatic flight manoeuvres and, in this regard, outperform any man-made autonomous flying system. To accomplish this extraordinary performance, flies shape actively by the specific succession of characteristic movements the dynamics of the image sequences on their eyes (‘optic flow’): They shift their gaze only from time to time by saccadic turns of body and head and keep it fixed between these saccades. Utilising the intervals of stable vision between saccades, an ensemble of motion-sensitive visual interneurons extracts from the optic flow information about different aspects of the self-motion of the animal and the spatial layout of the environment. This is possible in a computationally parsimonious way because the retinal image flow evoked by translational self-motion contains information about the spatial layout of the environment. Detection of environmental objects is even facilitated by adaptation mechanisms in the visual motion pathway. The consistency of our experimentally established hypotheses is tested by modelling the blowfly motion vision system and using this model to control the locomotion of a ‘Cyberfly’ moving in virtual environments. This CyberFly is currently being integrated in a robotic platform steering in three dimensions with a dynamics similar to that of blowflies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Baird, E., Srinivasan, M.V., Zhang. S., Cowling, A.: Visual control of flight speed in honeybees. The Journal of Experimental Biology 208, 3895–3905 (2005)

    Article  Google Scholar 

  2. Boeddeker, N., Egelhaaf, M.: Steering a virtual blowfly: Simulation of visual pursuit. Proceedings of the Royal Society of London B 270, 1971–1978 (2003)

    Google Scholar 

  3. Boeddeker, N., Kern, R., Egelhaaf, M.: Chasing a dummy target: Smooth pursuit and velocity control in male blowflies. Proceedings of the Royal Society of London B 270, 393–399 (2003)

    Google Scholar 

  4. Boeddeker, N., Lindemann, J.P., Egelhaaf, M., Zeil, J.: Responses of blowfly motion-sensitive neurons to reconstructed optic flow along outdoor flight paths. Journal of Comparative Physiology A 25, 1143–1155 (2005)

    Article  Google Scholar 

  5. Borst, A., Egelhaaf, M.: Principles of visual motion detection. Trends in Neurosciences 12, 297–306 (1989)

    Article  Google Scholar 

  6. Borst, A., Egelhaaf, M.: Detecting visual motion: Theory and models. In: F.A. Miles, J. Wallman (eds.) Visual motion and its role in the stabilization of gaze. Amsterdam: Elsevier (1993)

    Google Scholar 

  7. Borst, A., Haag, J.: Neural networks in the cockpit of the fly. Journal of Comparative Physiology A 188, 419–437 (2002)

    Article  Google Scholar 

  8. Dahmen, H.J., Franz, M.O., Krapp, H.G.: Extracting ego-motion from optic flow: limits of accuracy and neuronal filters. In: J.M. Zanker, J. Zeil (eds.) Computational, neural and ecological constraints of visual motion processing. Berlin, Heidelberg, New York, Springer (2000)

    Google Scholar 

  9. Douglass, J.K., Strausfeld, N.J.: Pathways in dipteran insects for early visual motion processing. In: J.M. Zanker, J. Zeil (eds.) Motion vision: computational, neural, and ecological constraints. Berlin, Heidelberg, New York, Springer; 67–81 (2001)

    Google Scholar 

  10. Egelhaaf, M.: The neural computation of visual motion. In: E. Warrant, D.-E. Nilsson (eds.) Invertebrate vision. Cambridge, UK, Cambridge University Press (2006)

    Google Scholar 

  11. Egelhaaf, M., Borst, A.: Motion computation and visual orientation in flies. Comparative Biochemistry and Physiology 104A, 659–673 (1993)

    Google Scholar 

  12. Egelhaaf, M., Borst, A.: Movement detection in arthropods. In: J. Wallman, F.A. Miles (eds.) Visual motion and its role in the stabilization of gaze. Amsterdam, London, New York, Elsevier, pp. 53–77 (1993)

    Google Scholar 

  13. Egelhaaf, M., Kern, R., Kurtz, R., Krapp, H.G., Kretzberg, J., Warzecha, A.-K: Neural encoding of behaviourally relevant motion information in the fly. Trends in Neurosciences 25, 96–102 (2002)

    Article  Google Scholar 

  14. Esch, H.E., Burns, J.M.: Distance estimation by foraging honeybees. The Journal of Experimental Biology 199, 155–162 (1996)

    Google Scholar 

  15. Esch, H.E. Zhang, S., Srinivasan, M.V., Tautz, J.: Honeybee dances communicate distances measured by optic flow. Nature 411, 581–583 (2001)

    Article  Google Scholar 

  16. Farina, W.M., Varjú, D., Zhou, Y: The regulation of distance to dummy flowers during hovering flight in the hawk moth Macroglossum stellatarum. Journal of Comparative Physiology 174, 239–247 (1994)

    Google Scholar 

  17. Farrow, K., Borst, A., Haag, J.: Sharing Receptive Fields with Your Neighbors: Tuning the Vertical System Cells to Wide Field Motion. Journal of Neuroscience 25, 3985–3993 (2005)

    Article  Google Scholar 

  18. Franceschini, N., Pichon, J.M., Blanes, C.: From insect vision to robot vision. Philosophical Transactions of the Royal Society of London. Series B 337, 283–294 (1992)

    Article  Google Scholar 

  19. Franz, M.O., Mallot, H.A.: Biomimetic robot navigation. Robots and Autonomous Systems, 133–153 (2000)

    Google Scholar 

  20. Frye, M.A., Dickinson, M.H.: Closing the loop between neurobiology and flight behavior in Drosophila. Current Opinion in Neurobiology 14, 729–736 (2004)

    Article  Google Scholar 

  21. Frye, M.A., Dickinson, M.H.: Visual edge orientation shapes free-flight behavior in Drosophila. Fly 1, 153–154 (2007)

    Google Scholar 

  22. Hausen, K.: Motion sensitive interneurons in the optomotor system of the fly. I. The Horizontal Cells: Structure and signals. Biological Cybernetics 45, 143–156 (1982)

    Article  Google Scholar 

  23. Hausen, K.: Motion sensitive interneurons in the optomotor system of the fly. II. The Horizontal Cells: Receptive field organization and response characteristics. Biological Cybernetics 46, 67–79 (1982)

    Article  Google Scholar 

  24. Hausen, K., Egelhaaf, M.: Neural mechanisms of visual course control in insects. In: D. Stavenga, R.C. Hardie (eds.) Facets of vision. Berlin, Heidelberg, New York, Springer; 391–424 (1989)

    Google Scholar 

  25. Hengstenberg, R.: Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. Journal of Comparative Physiology 149, 179–193 (1982)

    Article  Google Scholar 

  26. Hengstenberg, R., Hausen, K., Hengstenberg, B.: The number and structure of giant vertical cells (VS) in the Lobula plate of the blowfly, Calliphora erythrocephala. Journal of Comparative Physiology 149, 163–177 (1982)

    Article  Google Scholar 

  27. Hrncir, M., Jarau, S., Zucchi, R., Barth, F.G.: A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances. Journal of Comparative Physiology Series A 189, 761–768 (2003)

    Article  Google Scholar 

  28. Jain, A.K., Dubes, R.C.: Algorithms for clustering data. Prentice-Hall (1988)

    Google Scholar 

  29. Juusola, M., French, A.S., Uusitalo, R.O., Weckström, M.: Information processing by graded-potential transmission through tonically active synapses. Trends in Neurosciences 19, 292–297 (1996)

    Article  Google Scholar 

  30. Karmeier, K., van Hateren, J.H., Kern, R., Egelhaaf, M.: Encoding of naturalistic optic flow by a population of blowfly motion sensitive neurons. Journal of Neurophysiology 96, 1602–1614 (2006)

    Article  Google Scholar 

  31. Kern, R., van Hateren, J.H., Egelhaaf, M.: Representation of behaviourally relevant information by blowfly motion-sensitive visual interneurons requires precise compensatory head movements. Jounal of Experimental Biology 209, 1251–1260 (2006)

    Article  Google Scholar 

  32. Kern, R., van Hateren, J.H., Michaelis, C., Lindemann, J.P., Egelhaaf, M.: Function of a fly motion-sensitive neuron matches eye movements during free flight. PLOS Biology 3, 1130–1138 (2005)

    Article  Google Scholar 

  33. Kern, R., Varjú, D.: Visual position stabilization in the hummingbird hawk moth, Macroglossum stellatarum L.: I. Behavioural analysis. Journal of Comparative Physiology Series A 182, 225–237 (1998)

    Article  Google Scholar 

  34. Kimmerle, B., Srinivasan, M.V., Egelhaaf, M.: Object detection by relative motion in freely flying flies. Naturwiss 83, 380–381 (1996)

    Article  Google Scholar 

  35. Koenderink, J.J.: Optic Flow. Vision Research 26, 161–180 (1986)

    Article  Google Scholar 

  36. Köhler, T., Röchter, F., Lindemann, J.P., Möller, R.: Bio-inspired motion detection in an FPGA-based smart camera module Bioinspiration & Biomimimetics 4 (1:015008), 2009 doi: 10.1088/1748-3182/4/1/015008

    Google Scholar 

  37. Kral, K., Poteser, M.: Motion parallax as a source of distance information in locusts and mantids. Journal of Insect Behavior 10, 145–163 (1997)

    Article  Google Scholar 

  38. Krapp, H.G.: Neuronal matched filters for optic flow processing in flying insects. In: M. Lappe (ed.) Neuronal processing of optic flow. San Diego, San Francisco, New York, Academic Press, pp. 93–120 (2000)

    Google Scholar 

  39. Krapp, H.G., Hengstenberg, B., Hengstenberg, R.: Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. Journal of Neurophysiology 79, 1902–1917 (1998)

    Google Scholar 

  40. Krapp, H.G., Hengstenberg, R., Egelhaaf, M.: Binocular contribution to optic flow processing in the fly visual system. Journal of Neurophysiology 85, 724–734 (2001)

    Google Scholar 

  41. Land, M.F., Eckert, H.: Maps of the acute zones of fly eyes. Journal of Comparative Physiology Series A 156, 525–538 (1985)

    Article  Google Scholar 

  42. Lappe, M. Ed: Neuronal processing of optic flow. San Diego, San Francisco, New York, Academic Press (2000)

    Google Scholar 

  43. Laughlin, S.B: Matched filtering by a photoreceptor membrane. Vision Research 36, 1529–1541 (1996)

    Article  Google Scholar 

  44. Lehrer, M.: Small-scale navigation in the honeybee: Active acquisition of visual information about the goal. The Journal of Experimental Biology 199, 253–261 (1996)

    Google Scholar 

  45. Lehrer, M., Srinivasan, M.V., Zhang S.W., Horridge, G.A.: Motion cues provide the bee’s visual world with a third dimension. Nature 332, 356–357 (1988)

    Article  Google Scholar 

  46. Liang, P., Kern, R., Egelhaaf, M.: Motion adaptation facilitates object detection in three-dimensional environment. Journal of Neuroscience 29, 11328–1332 (2008)

    Google Scholar 

  47. Lindemann, J.P., Kern, R., Michaelis, C., Meyer, P., van Hateren, J.H., Egelhaaf, M.: FliMax, a novel stimulus device for panoramic and highspeed presentation of behaviourally generated optic flow. Vision Research 43, 779–791 (2003)

    Article  Google Scholar 

  48. Lindemann, J.P., Kern, R., van Hateren, J.H., Ritter, H., Egelhaaf, M.: On the computations analysing natural optic flow: Quantitative model analysis of the blowfly motion vision pathway. Journal of Neuroscience 25, 6435–6448 (2005)

    Article  Google Scholar 

  49. Lindemann, J.P., Weiss, H., Möller, R., Egelhaaf, M.: Saccadic flight strategy facilitates collision avoidance: Closed-loop performance of a cyberfly. Biological Cybernetics 98, 213–227 (2007)

    Article  Google Scholar 

  50. Longuet-Higgins, H.C., Prazdny, K.: The interpretation of a moving retinal image. Proceedings of the Royal Society of London. Series B 208, 385–397 (1980)

    Google Scholar 

  51. Neumann, T.R.: Biomimetic spherical vision. Universität Tübingen; 2004.

    Google Scholar 

  52. Petrowitz, R., Dahmen, H.J., Egelhaaf, M., Krapp, H.G.: Arrangement of optical axes and the spatial resolution in the compound eye of the female blowfly Calliphora. Journal of Comparative Physiology Series A 186, 737–746 (2000)

    Article  Google Scholar 

  53. Pfaff, M., Varjú, D.: Mechanisms of visual distance perception in the hawk moth Macroglossum stellatarum. Zoology Jb Physiology 95, 315–321 (1991)

    Google Scholar 

  54. Prazdny, K.: Ego-Motion and Relative Depth Map from Optical-Flow. Biological Cybernetics 36, 87–102 (1980)

    Article  MATH  MathSciNet  Google Scholar 

  55. Reiser, M.B., Dickinson, M.H.: A test bed for insect-inspired robotic control. Philosophical Transactions of the Royal Society of London. Series A 361, 2267–2285 (2003)

    Article  MathSciNet  Google Scholar 

  56. Schack, T.: The cognitive architecture of movement. International Journal of Sport & Exercise Psychology 2, 403–438 (2004)

    Google Scholar 

  57. Schilstra, C., van Hateren, J.H.: Stabilizing gaze in flying blowflies. Nature 395, 654 (1998)

    Article  Google Scholar 

  58. Schilstra, C., van Hateren, J.H.: Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics. The Journal of Experimental Biology 202, 1481–1490 (1999)

    Google Scholar 

  59. Sobey, P.J.: Active navigation with a monocular robot. Biological Cybernetics 71, 433–440 (1994)

    Article  Google Scholar 

  60. Srinivasan, M.V., Lehrer, M., Kirchner, W.H., Zhang, S.W.: Range perception through apparent image speed in freely flying honeybees. Visual Neuroscience 6, 519–535 (1991)

    Article  Google Scholar 

  61. Srinivasan, M.V., Lehrer, M., Zhang, S.W., Horridge, G.A.: How honeybees measure their distance from objects of unknown size. Journal of Comparative Physiology Series A 165, 605–613 (1989)

    Article  Google Scholar 

  62. Srinivasan, M.V., Zhang, S., Altwein, M., Tautz, J.: Honeybee navigation: Nature and calibration of the “odometer”. Science 287, 851–853 (2000)

    Article  Google Scholar 

  63. Srinivasan, M.V., Zhang, S.W., Lehrer, M., Collett, T.S.: Honeybee navigation en route to the goal: Visual flight control and odometry. The Journal of Experimental Biology 199, 237–244 (1996)

    Google Scholar 

  64. Strausfeld, N.J., Douglass, J.K, Campbell, H.R., Higgins, C.M.: Parallel processing in the optic lobes of flies and the occurrence of motion computing circuits. In: E. Warrant, D.-E. Nilsson (eds.) Invertebrate vision, pp. 349–398 Cambridge, Cambridge University Press (2006)

    Google Scholar 

  65. Tammero, L. F., Dickinson, M.H.: The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. The Journal of Experimental Biology 205, 327–343 (2002)

    Google Scholar 

  66. Tautz, J., Zhang, S., Spaethe, J., Brockmann, A., Si, A., Srinivasan, M.: Honeybee odometry: performance in varying natural terrain. PLOS Biology 2, 915–923 (2004)

    Article  Google Scholar 

  67. Thoroughman, K.A., Shadmehr, R.: Learning of action through adaptive combination of motor primitives. Nature 407, 742–747 (2000)

    Article  Google Scholar 

  68. Thurau, C., Bauckhage, C., Sagerer, G.: Synthesizing movements for computer game characters, pp. 179–1863175 Heidelberg, Springer (2004)

    Google Scholar 

  69. van Hateren, J.H.: Processing of natural time series of intensities by the visual system of the blowfly. Vision Research 37, 3407–3416 (1997)

    Article  Google Scholar 

  70. van Hateren, J.H., Schilstra, C.: Blowfly flight and optic flow. II. Head movements during flight. The Journal of Experimental Biology 202, 1491–1500 (1999)

    Google Scholar 

  71. Webb, B., Harrison, R.R., Willis, M.A.: Sensorimotor control of navigation in arthropod artifical systems. Arthropod Structure & Development 33, 301–329 (2004)

    Article  Google Scholar 

  72. Zeil, J.: Orientation flights of solitary wasps (Cerceris, Sphecidae, Hymenoptera). I. Description of flights. Journal of Comparative Physiology Series A 172, 189–205 (1993)

    Article  Google Scholar 

  73. Zeil, J.: Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera). II. Similarities between orientation and return flights and the use of motion parallax. Journal of Comparative Physiology Series A 172, 207–222 (1993)

    Article  Google Scholar 

  74. Zeil, J., Kelber, A., Voss, R.: Structure and function of learning flights in bees and wasps. The Journal of Experimental Biology 199, 245–252 (1997)

    Google Scholar 

  75. Zufferey, J.-C., Floreano, D,: Fly-Inspired Visual Steering of an Ultralight Indoor Aircraft. IEEE Transactions on Robotics 22, 137–146 (2006)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Egelhaaf .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Egelhaaf, M., Kern, R., Lindemann, J.P., Braun, E., Geurten, B. (2009). Active Vision in Blowflies: Strategies and Mechanisms of Spatial Orientation. In: Floreano, D., Zufferey, JC., Srinivasan, M., Ellington, C. (eds) Flying Insects and Robots. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89393-6_4

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-89393-6_4

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-89392-9

  • Online ISBN: 978-3-540-89393-6

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics