Visual motion speed determines a behavioral switch from forward flight to expansion avoidance in drosophila

Journal of Experimental Biology

Volumn 216, Issue 4, 2013, Pages 719-732

  Reiser, Michael B ^a   Dickinson, Michael H ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Elementary motion detector; Insect vision; Navigation; Visual expansion

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; AVOIDANCE BEHAVIOR; DROSOPHILA MELANOGASTER; FEMALE; FLYING; MOVEMENT PERCEPTION; ORIENTATION; PHOTOSTIMULATION; PHYSIOLOGY; TIME; VISION;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; FEMALE; FLIGHT, ANIMAL; MOTION PERCEPTION; ORIENTATION; PHOTIC STIMULATION; TIME FACTORS; VISUAL PERCEPTION;

EID: 84873418077     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.074732     Document Type: Article

References (55)

1. Bender, J. A. and Dickinson, M. H. (2006). A comparison of visual and halteremediated feedback in the control of body saccades in Drosophila melanogaster. J. Exp. Biol. 209, 4597-4606.
2. Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B Met. 57, 289-300.
3. Borst, A. and Bahde, S. (1987). Comparison between the movement detection systems underlying the optomotor and the landing response in the housefly. Biol. Cybern. 56, 217-224.
4. Borst, A. and Egelhaaf, M. (1989). Principles of visual motion detection. Trends Neurosci. 12, 297-306.
5. Borst, A., Reisenman, C. and Haag, J. (2003). Adaptation of response transients in fly motion vision. II: Model studies. Vision Res. 43, 1311-1324.
6. Büchner, E. (1974). Bewegungsperzeption in einem visuellen System mit gerastertem Eingang. PhD thesis, University of Tubingen, Germany.
7. Buchner, E. (1976). Elementary movement detectors in an insect visual system. Biol. Cybern. 24, 85-101.
8. Buchner, E. (1984). Behavioural analysis of spatial vision in insects. In Photoreception and Vision in Invertebrates (ed. M. A. Ali), pp. 561-621. New York: Plenum.
9. Budick, S. A. and Dickinson, M. H. (2006). Free-flight responses of Drosophila melanogaster to attractive odors. J. Exp. Biol. 209, 3001-3017.
10. Budick, S. A., Reiser, M. B. and Dickinson, M. H. (2007). The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster. J. Exp. Biol. 210, 4092-4103.
11. Burton, B. G. and Laughlin, S. B. (2003). Neural images of pursuit targets in the photoreceptor arrays of male and female houseflies Musca domestica. J. Exp. Biol. 206, 3963-3977.
12. Clark, D. A., Bursztyn, L., Horowitz, M. A., Schnitzer, M. J. and Clandinin, T. R. (2011). Defining the computational structure of the motion detector in Drosophila. Neuron 70, 1165-1177.
13. David, C. T. (1978). The relationship between body angle and flight speed in freeflying Drosophila. Physiol. Entomol. 3, 191-195.
14. David, C. T. (1982). Compensation for height in the control of groundspeed by Drosophila in a new, 'barber's pole' wind tunnel. J. Comp. Physiol. A 147, 485-493.
15. Duistermars, B. J., Chow, D. M., Condro, M. and Frye, M. A. (2007). The spatial, temporal and contrast properties of expansion and rotation flight optomotor responses in Drosophila. J. Exp. Biol. 210, 3218-3227.
16. Duistermars, B. J., Care, R. A. and Frye, M. A. (2012). Binocular interactions underlying the classic optomotor responses of flying flies. Frontiers 6, 6.
17. Franceschini, N., Ruffier, F. and Serres, J. (2007). A bio-inspired flying robot sheds light on insect piloting abilities. Curr. Biol. 17, 329-335.
18. Fry, S. N., Rohrseitz, N., Straw, A. D. and Dickinson, M. H. (2009). Visual control of flight speed in Drosophila melanogaster. J. Exp. Biol. 212, 1120-1130.
19. Frye, M. A., Tarsitano, M. and Dickinson, M. H. (2003). Odor localization requires visual feedback during free flight in Drosophila melanogaster. J. Exp. Biol. 206, 843-855.
20. Gibson, J. J. (1950). The Perception of the Visual World. Oxford: Houghton Mifflin.
21. Götz, K. G. (1968). Flight control in Drosophila by visual perception of motion. Kybernetik 4, 199-208.
22. Götz, K. G. (1975). Optomotor equilibrium of Drosophila navigation system. J. Comp. Physiol. A 99, 187-210.
23. Götz, K. G. (1987). Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J. Exp. Biol. 128, 35-46.
24. Götz, K. G. and Wandel, U. (1984). Optomotor control of the force of flight in Drosophila and Musca. Biol. Cybern. 51, 135-139.
25. Harris, R. A. and O'Carroll, D. C. (2002). Afterimages in fly motion vision. Vision Res. 42, 1701-1714.
26. Hassenstein, V. B. and Reichardt, W. (1956). Systemtheoretische Analyse der Zeit-, Reihenfolgen und Vorzeichenauswertung bei der Bewegungsperzeption des Russelkafers Chlorophanus. Z. Naturforschg. 11b, 513-524.
27. Hatsopoulos, N., Gabbiani, F. and Laurent, G. (1995). Elementary computation of object approach by wide-field visual neuron. Science 270, 1000-1003.
28. Hausen, K. and Wehrhahn, C. (1989). Neural circuits mediating visual flight control in flies. I. Quantitative comparison of neural and behavioral response characteristics. J. Neurosci. 9, 3828-3836.
29. Heisenberg, M. and Wolf, R. (1984). Vision in Drosophila: Genetics of Microbehavior. Berlin, Germany: Springer-Verlag.
30. Helmholtz, H. and Southall, J. (1925). Treatise on physiological optics. III. The Perceptions of Vision. New York: Optical Society of America.
31. Hengstenberg, R. (1991a). Head posture, body posture and gaze movements in the resting and flying fruitfly Drosophila. Synapse 1991, 273.
32. Hengstenberg, R. (1991b). Gaze control in the blowfly Calliphora: A multisensory, twostage integration process. Semin. Neurosci. 3, 19-29.
33. Kung, C. (1971). Genic mutants with altered system of excitation in Paramecium aurelia. II. Mutagenesis, screening and genetic analysis of the mutants. Genetics 69, 29-45.
34. Lappe, M., Bremmer, F. and van den Berg, A. V. (1999). Perception of self-motion from visual flow. Trends Cogn. Sci. 3, 329-336.
35. Laughlin, S. B. and Hardie, R. C. (1978). Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J. Comp. Physiol. 128, 319-340.
36. Lehmann, F. O. and Dickinson, M. H. (1997). The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. J. Exp. Biol. 200, 1133-1143.
37. Maimon, G., Straw, A. D. and Dickinson, M. H. (2008). A simple vision-based algorithm for decision making in flying Drosophila. Curr. Biol. 18, 464-470.
38. Nelson, M. E. and MacIver, M. A. (2006). Sensory acquisition in active sensing systems. J. Comp. Physiol. A 192, 573-586.
39. Reichardt, W. (1961). Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In Sensory Communication (ed. W. A. Rosenblith), pp. 303-317. Cambridge, MA: MIT Press.
40. Reiff, D. F., Plett, J., Mank, M., Griesbeck, O. and Borst, A. (2010). Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nat. Neurosci. 13, 973-978.
41. Reiser, M. B. (2006). Visually mediated control of flight in Drosophila: Not lost in translation. PhD thesis, California Institute of Technology, Pasadena, CA, USA.
42. Reiser, M. B. and Dickinson, M. H. (2008). A modular display system for insect behavioral neuroscience. J. Neurosci. Methods 167, 127-139.
43. Reiser, M. B. and Dickinson, M. H. (2010). Drosophila fly straight by fixating objects in the face of expanding optic flow. J. Exp. Biol. 213, 1771-1781.
44. Robertson, R. M. and Reye, D. N. (1992). Wing movements associated with collision avoidance manoeuvres during flight in the locust Locusta migratoria. J. Exp. Biol. 163, 231-258.
45. Sandeman, D. C. and Markl, H. (1980). Head movements in flies (Calliphora) produced by deflexion of the halteres. J. Exp. Biol. 85, 43-60.
46. Snyder, A. W. (1979). Physics of vision in compound eyes. Handb. Sens. Physiol. 7, 225-313.
47. Srinivasan, M. V., Lehrer, M., Kirchner, W. H. and Zhang, S. W. (1991). Range perception through apparent image speed in freely flying honeybees. Vis. Neurosci. 6, 519-535.
48. Stewart, F. J., Baker, D. A. and Webb, B. (2010). A model of visual-olfactory integration for odour localisation in free-flying fruit flies. J. Exp. Biol. 213, 1886-1900.
49. Tammero, L. F. and Dickinson, M. H. (2002). The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. J. Exp. Biol. 205, 327-343.
50. Tammero, L. F., Frye, M. A. and Dickinson, M. H. (2004). Spatial organization of visuomotor reflexes in Drosophila. J. Exp. Biol. 207, 113-122.
51. van Hateren, J. H. and Schilstra, C. (1999). Blowfly flight and optic flow. II. Head movements during flight. J. Exp. Biol. 202, 1491-1500.
52. Wagner, H. (1982). Flow-field variables trigger landing in flies. Nature 297, 147-148.
53. Wang, Y. and Frost, B. J. (1992). Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature 356, 236-238.
54. Warzecha, A. K. and Egelhaaf, M. (1996). Intrinsic properties of biological motion detectors prevent the optomotor control system from getting unstable. Philos. Trans. R. Soc. B 351, 1579-1591.
55. Zanker, J. M., Egelhaaf, M. and Warzecha, A.-K. (1991). On the coordination of motor output during visual flight control of flies. J. Comp. Physiol. A 169, 127-134.