Chasing behavior and optomotor following in free-flying male blowflies: Flight performance and interactions of the underlying control systems

Frontiers in Behavioral Neuroscience

Volumn 4, Issue , 2010, Pages

  Trischler, Christine ^a   Kern, Roland ^a   Egelhaaf, Martin ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Control systems; Eye movements; Fl y; Optomotor following; Saccade; Visual pursuit

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BLOWFLY; CONTROLLED STUDY; EYE TRACKING; FEEDBACK SYSTEM; FLIGHT; FLY; FLYING; GAZE; MALE; NONHUMAN; SACCADIC EYE MOVEMENT; VISUAL DISCRIMINATION; VISUOMOTOR COORDINATION;

EID: 77953410086     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2010.00020     Document Type: Article

References (92)

1. Barnett, P. D., Nordström, K., and O'Carroll, D. C. (2007). Retinotopic organization of small-field-targetdetecting neurons in the insect visual system. Curr. Biol. 17, 1-10.
2. Boeddeker, N., and Egelhaaf, M. (2003). Steering a virtual blowfl y: Simulation of visual pursuit. Proc. R. Soc. Lond., B, Biol. Sci. 270, 1971-1978.
3. Boeddeker, N., and Egelhaaf, M. (2005). Chasing behaviour of blowflies: a smooth pursuit system generates saccades. J. Exp. Biol. 208, 1563-1572.
4. Boeddeker, N., Kern, R., and Egelhaaf, M. (2003). Chasing a dummy target: smooth pursuit and velocity control in male blowflies. Proc. R. Soc. Lond., B, Biol. Sci. 270, 393-399.
5. Böhm, H., Schildberger, K., and Huber, F. (1991). Visual and acoustic course control in the cricket Gryllus bimaculatus. J. Exp. Biol. 159, 235-248.
6. Borst, A., and Bahde, S. (1987). Comparison between the movement detection systems underlying the optomotor and the landing response in the housefl y. Biol. Cybern. 56, 217-224.
7. Collett, T. S. (1980). Angular tracking and the optomotor response. An analysis of visual refl ex interaction in a hoverfl y. J. Comp. Physiol. 140, 145-158.
8. Collett, T. S., and Land, M. F. (1975). Visual control of fl ight behaviour in the hoverfl y Syritta pipiens L. J. Comp. Physiol. 99, 1-66.
9. Collett, T. S., Nalbach, H.-O., and Wagner, H. (1993). "Visual stabilization in arthropods," in Visual Motion and its Role in the Stabilization of Gaze, eds F. A. Miles and J. Wallman (Amsterdam/London/ New York: Elsevier), 239-264.
10. Collewijn, H., and Tamminga, E. P. (1984). Human smooth and saccadic eyemovements during voluntary pursuit of different target motions on different backgrounds. J. Physiology. 351, 217-250.
11. Crapse, T. B., and Sommer, M. A. (2008). Corollary discharge across the animal kingdom. Nat. Rev. Neurosci. 9, 587-600.
12. De Brouwer, S., Missal, M., and Lefevre, P. (2001). Role of retinal slip in the prediction of target motion during smooth and saccadic pursuit. J. Neurophysiol. 86, 550-558.
13. De Brouwer, S., Yuksel, D., Blohm, G., Missal, M., and Lefevre, P. (2002). What triggers catch-up saccades during visual tracking? J. Neurophysiol. 87, 1646-1650.
14. Duistermars, B. J., Reiser, M. B., Zhu, Y., and Frye, M. A. (2007). Dynamic properties of large-fi eld and small-fi eld optomotor fl ight responses in Drosophila. J. Comp. Physiol. A 193, 787-799.
15. Egelhaaf, M. (1987). Dynamic properties of two control systems underlying visually guided turning in house-fl ies. J. Comp. Physiol. A 161, 777-783.
16. Egelhaaf, M. (1989). Visual afferences to flight steering muscles controlling optomotor response of the fl y. J. Comp. Physiol. A 165, 719-730.
17. Egelhaaf, M. (2009). Insect motion vision. Scholarpedia 4, 1671.
18. Egelhaaf, M., Hausen, K., Reichardt, W., and Wehrhahn, C. (1988). Visual course control in fl ies relies on neuronal computation of object and background motion. Trends Neurosci. 11, 351-358.
19. Frye, M. A., and Olberg, R. M. (1995). Visual receptive-field properties of feature detecting neurons in the dragonfly. J. Comp. Physiol. A 177, 569-576.
20. Gardner, J. L., and Lisberger, S. G. (2001). Linked target selection for saccadic and smooth pursuit eye movements. J. Neurosci. 21, 2075-2084.
21. Gilbert, C., and Strausfeld, N. J. (1991). The functional organization of malespecifi c visual neurons in fl ies. J. Comp. Physiol. A 169, 395-411.
22. Götz, K. G. (1968). Flight control in Drosophila by visual perception of motion. Kybernetik 4, 199-208.
23. Gries, M., and Koeniger, N. (1996). Straight forward to the queen: pursuing honeybee drones (Apis mellifera L) adjust their body axis to the direction of the queen. J. Comp. Physiol. A 179, 539-544.
24. Hardie, R. C. (1985). "Functional organization of the fl y retina," in Progress in Sensory Physiology, Vol. 5, eds H. Autrum, D. Ottoson, E. R. Perl, R. F. Schmidt, H. Shimazu and W. D. Willis (Berlin/Heidelberg/New York/Tokyo: Springer), 1-79.
25. Hausen, K. (1982a). Motion sensitive interneurons in the optomotor system of the fl y. I. The horizontal cells: structure and signals. Biol. Cybern. 45, 143-156.
26. Hausen, K. (1982b). Motion sensitive interneurons in the optomotor system of the fl y. II. The horizontal cells: receptive fi eld organization and response characteristics. Biol. Cybern. 46, 67-79.
27. Hausen, K., and Egelhaaf, M. (1989). "Neural mechanisms of visual course control in insects," in Facets of Vision, eds D. Stavenga and R. C. Hardie (Berlin/Heidelberg/New York: Springer), 391-424.
28. Hausen, K., and Strausfeld, N. J. (1980). Sexually dimorphic interneuron arrangements in the fl y visual system. Proc. R. Soc. Lond., B, Biol. Sci. 208, 57-71.
29. Heisenberg, M., and Wolf, R. (1984). Vision in Drosophila. Berlin/Heidelberg/New York/Tokyo: Springer. Hengstenberg, R. (1993). "Multisensory control in insect oculomotor systems," in Visual Motion and its Role in the Stabilization of Gaze, eds F. A. Miles and J. Wallman (Amsterdam/Tokyo/New York/London: Elsevier), 285-298.
30. Ilg, U. J. (1997). Slow eye movement. Prog. Neurobiol. 53, 293-329.
31. Karmeier, K., van Hateren, J. H., Kern, R., and Egelhaaf, M. (2006). Encoding of naturalistic optic fl ow by a population of blowfl y motion sensitive neurons. J. Neurophysiol. 96, 1602-1614.
32. Keller, E. L., and Khan, N. S. (1986). Smooth-pursuit initiation in the presence of a textured background in monkey. Vision Res. 26, 943-955.
33. Kern, R., and Egelhaaf, M. (2000). Optomotor course control in flies with largely asymmetric visual input. J. Comp. Physiol. A 186, 45-55.
34. Kern, R., van Hateren, J. H., and Egelhaaf, M. (2006). Representation of behaviourally relevant information by blowfly motion-sensitive visual interneurons requires precise compensatory head movements. J. Exp. Biol. 209, 1251-1260.
35. Kern, R., van Hateren, J. H., Michaelis, C., Lindemann, J. P., and Egelhaaf, M. (2005). Function of a fl y motionsensitive neuron matches eye movements during free flight. PLoS Biol. 3, 1130-1138. doi:10.1371/journal. pbio.0030171.
36. Kimmerle, B., Srinivasan, M. V., and Egelhaaf, M. (1996). Object detection by relative motion in freely fl ying fl ies. Naturwissenschaften 83, 380-381.
37. Kimmerle, B., Warzecha, A.-K., and Egelhaaf, M. (1997). Object detection in the fl y during simulated translatory fl ight. J. Comp. Physiol. A 181, 247-255.
38. Kimmig, H., Miles, F. A., and Schwarz, U. (1992). Effect of stationary textured backgrounds on the initiation of smooth pursuit eye-movements in monkey. J. Neurosci. 68, 2147-2164.
39. Kirschfeld, K. (1997). "Course control and tracking: orientation through image stabilization," in Orientation and Communication in Arthropods, ed. M. Lehrer (Basel: Birkhäuser), 67-93.
40. Kral, K. (2003). Behavioural-analytical studies of the role of head movements in depth perception in insects, birds and mammals. Behav. Processes 64, 1-12.
41. Krauzlis, R. J. (2004). Recasting the smooth pursuit eye movement system. J. Neurophysiol. 91, 591-603.
42. Land, M. F. (1993a). Chasing and pursuit in the dolichopodid fl y Poecilobothrus nobilitatus. J. Comp. Physiol. A 173, 605-613.
43. Land, M. F. (1993b). The visual control of courtship in the fl y Poecilobothrus nobilitatus. J. Comp. Physiol. A 173, 595-603.
44. Land, M. F. (1999). Motion and vision: why animals move their eyes. J. Comp. Physiol. A 185, 341-352.
45. Land, M. F., and Collett, T. S. (1974). Chasing behaviour of houseflies (Fannia canicularis). A description and analysis. J. Comp. Physiol. 89, 331-357.
46. Land, M. F., and Collett, T. S. (1997). "A survey of active vision in invertebrates," in From Living Eyes to Seeing Machines, eds M.V. Srinivasan and S. Venkatesh (Oxford: Oxford University Press), 16-36.
47. Land, M. F., and Eckert, H. (1985). Maps of the acute zones of fl y eyes. J. Comp. Physiol. A 156, 525-538.
48. Land, M. F., and McLeod, P. (2000). From eye movements to actions: how batsmen hit the ball. Nat. Neurosci. 3, 1340-1345.
49. Lindemann, J. P. (2006). Visual Navigation of a Virtual Blowfly. Doctoral thesis, Bielefeld University. URL: http://bieson.ub.uni-bielefeld.de/volltexte/2006/897/
50. Lindemann, J. P., Kern, R., van Hateren, J. H., Ritter, H., and Egelhaaf, M. (2005). On the computations analysing natural optic fl ow: quantitative model analysis of the blowfl y motion vision pathway. J. Neurosci. 25, 6435-6448.
51. Lindemann, J. P., Weiss, H., Möller, R., and Egelhaaf, M. (2007). Saccadic fl ight strategy facilitates collision avoidance: closed-loop performance of a cyberfl y. Biol. Cybern. 98, 213-227.
52. Masson, G., Proteau, L., and Mestre, D. R. (1995). Effects of stationary and moving textured backgrounds on the visuo-oculo-manual tracking in humans. Vision Res. 35, 837-852.
53. McBeath, M. K., Shaffer, D. M., and Kaiser, M. K. (1995). How baseball outfi elders determine where to run to catch fl y balls. Science 268, 569-573.
54. Miles, F. A. (1997). Visual stabilization of the eyes in primates. Curr. Opin. Neurobiol. 7, 867-871.
55. Miles, F. A., and Wallman, J. E. (1993). Visual Motion and its Role in the Stabilization of Gaze. Amsterdam/ London/New York: Elsevier.
56. Mohrmann, H., and Thier, P. (1995). The influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and smooth-pursuit termination. Biol. Cybern. 73, 83-93.
57. Mronz, M., and Lehmann, F. O. (2008). The free-fl ight response of Drosophila to motion of the visual environment. J. Exp. Biol. 211, 2026-2045.
58. Niemann, T., and Hoffmann, K.-P. (1997). Motion processing for saccadic eye movements during the visually induced sensation of egomotion in humans. Vision Res. 37, 3163-3170.
59. Nordström, K., Barnett, P. D., and O'Carroll, D. C. (2006). Insect detection of small targets moving in visual clutter. PLoS Biol. 4, 378-386. doi:10.1371/journal.pbio.0040054.
60. Nordström, K., and O'Carroll, D. C. (2006). Small object detection neurons in female hoverfl ies. Proc. R. Soc. Lond., B, Biol. Sci. 273, 1211-1216.
61. O'Carroll D. C. (1993). Feature- detecting neurons in dragonfl ies. Nature 362, 541-543.
62. Olberg, R. M. (1981). Object- and selfmovement detectors in the ventral nerve cord of the dragonfl y. J. Comp. Physiol. 141, 327-334.
63. Olberg, R. M., Worthington, A. H., Fox, J. L., Bessette, C. E., and Loosemore, M. P. (2005). Prey size selection and distance estimation in foraging adult dragonfl ies. J. Comp. Physiol. A 191, 791-797.
64. Olberg, R. M., Worthington, A. H., and Venator, K. R. (2000). Prey pursuit and interception in dragonfl ies. J. Comp. Physiol. A 186, 155-162.
65. Orban de Xivry, J.-J., and Lefèvre, P. (2007). Saccades and pursuit: two outcomes of a single sensorimotor process. J. Physiol. 584, 11-23.
66. Reichardt, W., Poggio, T., and Hausen, K. (1983). Figure-ground discrimination by relative movement in the visual system of the fl y. Part II: Towards the neural circuitry. Biol. Cybern. 46(Suppl.), 1-30.
67. Rossel, S. (1980). Foveal fixation and tracking in praying mantis. J. Comp. Physiol. 139, 307-331.
68. Schilstra, C., and van Hateren, J. H. (1999). Blowfl y fl ight and optic fl ow. I. Thorax kinematics and fl ight dynamics. J. Exp. Biol. 202, 1481-1490.
69. Schweigart, G., Mergner, T., Evdokimidis, I., Morand, S., and Becker, W. (1997). Gaze stabilization by optokinetic refl ex (OKR) and vestibulo-ocular reflex (VOR) during active head rotation in man. Vision Res. 37, 1643-1652.
70. Shaffer, D. M., and McBeath, M. K. (2002). Baseball outfielders maintain a linear optical trajectory when tracking uncatchable fl y balls. J. Exp. Psychol. Hum. Percept. Perform. 28, 335-348.
71. Sherman, A., and Dickinson, M. H. (2003). A comparison of visual and halteremediated equilibrium refl exes in the fruit fl y Drosophila melanogaster. J. Exp. Biol. 206, 295-302.
72. Spering, M., and Gegenfurtner, K. R. (2007). Contrast and assimilation in motion perception and smooth pursuit eye movements. J. Neurophysiol. 98, 1355-1363.
73. Srinivasan, M. V., Lehrer, M., Kirchner, W. H., and Zhang, S. W. (1991). Range perception through apparent image speed in freely fl ying honeybees. Vis. Neurosci. 6, 519-535.
74. Stout, J., Atkins, G., Weber, T., and Huber, F. (1987). The effect of visual input on calling song attractiveness for female Acheta domesticus. Physiol. Entomol. 12, 135-140.
75. Strausfeld, N. J. (1991). Structural organization of male-specifi c visual neurons in calliphorid optic lobes. J. Comp. Physiol. A 169, 379-393.
76. Strauss, R., and Heisenberg, M. (1990). "Gaze stabilizing head movements compensate for walk-induced body oscillations in the fly Drosophila melanogaster," in Brain-Perception- Cognition, eds N. Elsner and G. Roth (Stuttgart/New York: Thieme), 63.
77. Tammero, L. F., and Dickinson, M. H. (2002). The infl uence of visual landscape on the free fl ight behavior of the fruit fl y Drosophila melanogaster. J. Exp. Biol. 205, 327-343.
78. Trischler, C. (2009). Chasing Control in Male Blowflies: Behavioural Performance and Neuronal Responses. Doctoral dissertation, Bielefeld University. URL: http://bieson.ub.unibielefeld.de/volltexte/2009/1432/
79. Trischler, C., Boeddeker, N., and Egelhaaf, M. (2007). Characterisation of a blowfl y male-specifi c neuron using behaviourally generated visual stimuli. J. Comp. Physiol. A 193, 559-572.
80. van Hateren, J. H., and Schilstra, C. (1999). Blowfl y fl ight and optic fl ow. II. Head movements during fl ight. J. Exp. Biol. 202, 1491-1500.
81. Virsik, R., and Reichardt, W. (1976). Detection and tracking of moving objects by the fly Musca domestica. Biol. Cybern. 23, 83-98.
82. von Holst, E., and Mittelstaedt, H. (1950). Das Reafferenzprinzip (Wechselwirkungen zwischen Zentralnervensystem und Peripherie). Naturwissenschaften 37, 464-476.
83. Wachenfeld, A., and Hausen, K. (1993). Functional characterization of the male lobula giant neuron 1 (MLG1) in the blowfl y, Calliphora erythrocephala (Meig.), in Göttingen Neurobiology Report, eds N. Elsner and M. Heisenberg (Stuttgart/New York: Thieme), 359.
84. Wachenfeld, A., and Hausen, K. (1994). "The role of male-specific visual interneurons in the mating behavior of the blowfl y, Calliphora erythrocephala (Meig.)," in Göttingen Neurobiology Report, eds N. Elsner and H. Breer (Stuttgart/New York: Thieme), 440.
85. Wagner, H. (1986a). Flight performance and visual control of fl ight of the freefl ying housefl y (Musca domestica). I. Organization of the flight motor. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 312, 527-551.
86. Wagner, H. (1986b). Flight performance and visual control of flight of the free-fl ying housefl y (Musca domestica). II. Pursuit of targets. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 312, 553-579.
87. Wagner, H. (1986c). Flight performance and visual control of fl ight of the freefl ying housefl y (Musca domestica). III. Interactions between angular movement induced by wide- and smallfi eld stimuli. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 312, 581-595.
88. 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. Lond., B, Biol. Sci. 351, 1579-1591.
89. Webb, B., Harrison, R. R., and Willis, M. A. (2004). Sensorimotor control of navigation in arthropod artifi cial systems. Arthropod Struct. Dev. 33, 301-329.
90. Weber, T., Atkins, G., Stout, J., and Huber, F. (1987). Female Acheta domesticus track acoustical and visual targets with different walking modes. Physiol. Entomol. 12, 141-147.
91. Wehner, R. (1981). "Spatial vision in arthropods," in Handbook of Sensory Physiology, Vol. VII/6C, Comparative Physiology and Evolution of Vision in Invertebrates, ed. H. Autrum (Berlin/Heidelberg/New York: Springer), 287-616.
92. Zeil, J. (1983). Sexual dimorphism in the visual system of flies: the free flight behaviour of male Bibionidae (Diptera). J. Comp. Physiol. A 150, 395-412.