Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila

PLoS Computational Biology

Volumn 9, Issue 2, 2013, Pages

  Censi, Andrea ^a   Straw, Andrew D ^b   Sayaman, Rosalyn W ^a   Murray, Richard M ^a   Dickinson, Michael H ^c  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STOCHASTIC SYSTEMS;

COMPLEX SEARCHES; DROSOPHILLA; DROSOPHILLA MELANOGASTER; EXTERNAL CAUSE; EXTERNAL STIMULUS; INTERNAL CAUSE; SCALAR VALUES; SEARCH ALGORITHMS; SENSORY CUES; VISUAL STIMULUS;

ANIMALS;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DECISION MAKING; DROSOPHILA MELANOGASTER; EYE TRACKING; FEMALE; FLYING; MALE; MATHEMATICAL MODEL; MOVEMENT PERCEPTION; NONHUMAN; PREDICTION; QUANTITATIVE ANALYSIS; RECEPTIVE FIELD; SACCADIC EYE MOVEMENT; STIMULUS RESPONSE; VISUAL DISCRIMINATION; VISUAL ORIENTATION; VISUAL STIMULATION;

EID: 84874777277     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002891     Document Type: Article

References (83)

1. Berg HC, Brown DA, (1972) Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking. Nature 239: 500-504.
2. Tynan CT, (1998) Ecological importance of the Southern Boundary of the Antarctic Circumpolar Current. Nature 392: 708-710 doi:10.1038/33675.
3. Fuortes MG, Yeandle S, (1964) Probability of occurrence of discrete potential waves in the eye of Limulus. The Journal of general physiology 47: 443-63.
4. Baylor DA, Lamb TD, Yau KW, (1979) Responses of retinal rods to single photons. The Journal of physiology 288: 613-34.
5. Menini A, Picco C, Firestein S, (1995) Quantal-like current fluctuations induced by odorants in olfactory receptor cells. Nature 373: 435-7 doi:10.1038/373435a0.
6. Shimada I, Kawazoe Y, Hara H, (1993) A temporal model of animal behavior based on a fractality in the feeding of Drosophila melanogaster. Biological Cybernetics 68: 477-481.
7. Cole B, Cole J, (1995) Fractal time in animal behaviour: the movement activity of Drosophila. Animal Behaviour 50: 1317-1324 doi:10.1016/0003-3472(95)80047-6.
8. Bartumeus F, Levin SA, (2008) Fractal reorientation clocks: Linking animal behavior to statistical patterns of search. Proceedings of the National Academy of Sciences 105: 19072.
9. Viswanathan GM, Afanasyev V, Buldyrev SV, Murphy EJ, Prince PA, et al. (1996) Lévy flight search patterns of wandering albatrosses. Nature 381: 413-415 doi:10.1038/381413a0.
10. Bartumeus F, Peters F, Pueyo S, Marrasé C, Catalan J, (2003) Helical L{é}vy walks: adjusting searching statistics to resource availability in microzooplankton. Proceedings of the National Academy of Sciences 100: 12771.
11. Humphries NE, Queiroz N, Dyer JRM, Pade NG, Musyl MK, et al. (2010) Environmental context explains Lévy and Brownian movement patterns of marine predators. Nature 465: 1066-1069 doi:10.1038/nature09116.
12. Maye A, Hsieh C-H, Sugihara G, Brembs B, (2007) Order in spontaneous behavior. PloS one 2: e443 doi:10.1371/journal.pone.0000443.
13. Reynolds AM, Frye Ma, (2007) Free-flight odor tracking in Drosophila is consistent with an optimal intermittent scale-free search. PloS one 2: e354 doi:10.1371/journal.pone.0000354.
14. Reynolds AM, Smith AD, Reynolds DR, Carreck NL, Osborne JL, (2007) Honeybees perform optimal scale-free searching flights when attempting to locate a food source. Journal of Experimental Biology 4: 3763-3770 doi:10.1242/jeb.009563.
15. Osborne JL, Andrew P, Carreck NL, Swain JL, Knight ME, et al. (2008) Bumblebee flight distances in relation to the forage landscape. Journal of Animal Ecology 77: 406-415 doi:10.1111/j.1365-2656.2007.01333.x.
16. Nevitt Ga, Losekoot M, Weimerskirch H, (2008) Evidence for olfactory search in wandering albatross, Diomedea exulans. Proceedings of the National Academy of Sciences of the United States of America 105: 4576-4581 doi:10.1073/pnas.0709047105.
17. Sims DW, Southall EJ, Humphries NE, Hays GC, Bradshaw CJA, et al. (2008) Scaling laws of marine predator search behaviour. Nature 451: 1098-1102 doi:10.1038/nature06518.
18. Nathan R, (2008) An emerging movement ecology paradigm. Proceedings of the National Academy of Sciences 105: 19050.
19. Reynolds A, (2008) How many animals really do the Lévy walk? Comment. Ecology 89: 2347-2351.
20. Stumpf MPH, Porter MA, (2012) Critical Truths About Power Laws. Science 335: 665-666 doi:10.1126/science.1216142.
21. Edwards AM, Phillips Ra, Watkins NW, Freeman MP, Murphy EJ, et al. (2007) Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449: 1044-8 doi:10.1038/nature06199.
22. Bartumeus F, (2007) Lévy processes in animal movement: an evolutionary hypothesis. Fractals 15: 151.
23. Goldreich O (2001) Foundations of Cryptography: Basic Tools. Cambridge University Press.
24. Hassenstein B, Reichardt W, (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkafers \emph{Chlorophanus}. Zeitschrift Für Naturforschung 11b: 513-524.
25. Srinivasan MV, Zhang SW, Lehrer M, Collett TS, (1996) Honeybee navigation en route to the goal: Visual flight control and odometry. Journal of Experimental Biology 199: 237-244.
26. Reynolds AM, Frye MA, (2007) Free-flight odor tracking in Drosophila is consistent with an optimal intermittent scale-free search. PloS one 2: e354 doi:10.1371/journal.pone.0000354.
27. Maye A, Hsieh C-H, Sugihara G, Brembs B, (2007) Order in spontaneous behavior. PloS one 2: e443 doi:10.1371/journal.pone.0000443.
28. Srivastava N, Clark DA, Samuel ADT, (2009) Temporal Analysis of Stochastic Turning Behavior of Swimming C. elegans. Journal of Neurophysiology pp. 1172-1179 doi:10.1152/jn.90952.2008.
29. Edwards AM, Phillips RA, Watkins NW, Freeman MP, Murphy EJ, et al. (2007) Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449: 1044-8 doi:10.1038/nature06199.
30. Nevitt Ga, Losekoot M, Weimerskirch H, (2008) Evidence for olfactory search in wandering albatross, Diomedea exulans. Proceedings of the National Academy of Sciences of the United States of America 105: 4576-81 doi:10.1073/pnas.0709047105.
31. Berg HC, Brown DA, (1972) Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking. Nature 239: 500-504.
32. Piggott BJ, Liu J, Feng Z, Wescott SA, Xu XZS, (2011) The Neural Circuits and Synaptic Mechanisms Underlying Motor Initiation in C. elegans. Cell 147: 922-933 doi:10.1016/j.cell.2011.08.053.
33. Kawano T, Po MD, Gao S, Leung G, Ryu WS, et al. (2011) An Imbalancing Act: Gap Junctions Reduce the Backward Motor Circuit Activity to Bias C. elegans for Forward Locomotion. Neuron 72: 572-86 doi:10.1016/j.neuron.2011.09.005.
34. Cowan NJ, Fortune ES, (2007) The critical role of locomotion mechanics in decoding sensory systems. The Journal of neuroscience: the official journal of the Society for Neuroscience 27: 1123-8 doi:10.1523/JNEUROSCI.4198-06.2007.
35. Beyeler A, Zufferey J-C, Floreano D, (2009) Vision-based control of near-obstacle flight. Autonomous Robots 27: 201-219 doi:10.1007/s10514-009-9139-6.
36. Conroy J, Gremillion G, Ranganathan B, Humbert JS, (2009) Implementation of wide-field integration of optic flow for autonomous quadrotor navigation. Autonomous Robots pp. 1-10.
37. Borst A, Euler T, (2011) Seeing things in motion: models, circuits, and mechanisms. Neuron 71: 974-94 doi:10.1016/j.neuron.2011.08.031.
38. Borst A, (2009) Drosophila's view on insect vision. Current biology 19: R36-47 doi:10.1016/j.cub.2008.11.001.
39. Kennedy JS, (1940) The visual responses of flying mosquitoes. Proceedings of the Zoological Society of London Series A 109: 221-242 doi:10.1111/j.1096-3642.1940.tb00831.x.
40. Mittelstaedt H, (1949) Telotaxis und Optomotorik von Eristalis bei Augeninversion. Naturwissenschaften 36: 90-91.
41. Eichner H, Joesch M, Schnell B, Reiff DF, Borst A, (2011) Internal structure of the fly elementary motion detector. Neuron 70: 1155-64 doi:10.1016/j.neuron.2011.03.028.
42. Clark DA, Bursztyn L, Horowitz MA, Schnitzer MJ, Clandinin TR, (2011) Defining the computational structure of the motion detector in Drosophila. Neuron 70: 1165-77 doi:10.1016/j.neuron.2011.05.023.
43. Reiff DF, Plett J, Mank M, Griesbeck O, Borst A, (2010) Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nature neuroscience 13: 973-978 doi:10.1038/nn.2595.
44. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A, (2010) ON and OFF pathways in Drosophila motion vision. Nature 468: 300-304 doi:10.1038/nature09545.
45. Krapp HG, Hengstenberg R, (1996) Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384: 463-6 doi:10.1038/384463a0.
46. Roth E, Reiser MB, Dickinson MH, Cowan NJ (2012) A Task-level Model for Optomotor Yaw Regulation in Drosophila Melanogaster: A Frequency-Domain System Identification Approach. In: Proceedings of the Conference on Decisions and Controls (CDC), Maui, Hawaii.
47. Aptekar JW, Shoemaker PA, Frye MA, (2012) Figure Tracking by Flies Is Supported by Parallel Visual Streams. Current biology 22: 482-487 doi:10.1016/j.cub.2012.01.044.
48. Theobald JC, Ringach DL, Frye MA, (2010) Dynamics of optomotor responses in Drosophila to perturbations in optic flow. The Journal of experimental biology 213: 1366-75 doi:10.1242/jeb.037945.
49. Mronz M, Lehmann F-O, (2008) The free-flight response of Drosophila to motion of the visual environment. The Journal of experimental biology 211: 2026-45 doi:10.1242/jeb.008268.
50. Braun E, Geurten B, Egelhaaf M, (2010) Identifying prototypical components in behaviour using clustering algorithms. PloS one 5: e9361 doi:10.1371/journal.pone.0009361.
51. Lindemann JP, Weiss H, Möller R, Egelhaaf M, (2008) Saccadic flight strategy facilitates collision avoidance: closed-loop performance of a cyberfly. Biological Cybernetics 98: 213-227 doi:10.1007/s00422-007-0205-x.
52. Boeddeker N, Egelhaaf M, (2005) A single control system for smooth and saccade-like pursuit in blowflies. J Exp Biol 208: 1563-1572 doi:10.1242/jeb.01558.
53. Land MF, Collett TS, (1974) Chasing behavior of houseflies (Fannia canicularis): a description and analysis. J Comp Physiol 89: 331-357.
54. Wagner H, (1986) Flight performance and visual control of the flight of the free-flying housefly (Musca domestica). II. Pursuit of targets. Philos Trans R Soc Long B Biol Sci 312: 553-579.
55. Tammero LF, Dickinson MH, (2002) The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. Journal of Experimental Biology 205: 327-343.
56. Stewart FJ, Baker DA, Webb B, (2010) A model of visual-olfactory integration for odour localisation in free-flying fruit flies. Journal of Experimental Biology 213: 1886-1900 doi:10.1242/jeb.026526.
57. Stephens GJ, Osborne LC, Bialek W, (2010) Searching for simplicity: Approaches to the analysis of neurons and behavior. Proc Natl Acad Sci U S A 108: 15565-71.
58. Heisenberg M, Wolf R (1984) Vision in Drosophila: genetics of Microbehavior. Springer-Verlag.
59. Straw AD, Branson K, Neumann TR, Dickinson MH, (2011) Multi-camera Realtime 3D Tracking of Multiple Flying Animals. J R Soc Interface 8: 395-409 doi:10.1098/rsif.2010.0230.
60. Breugel F, van Dickinson M, (2012) The visual control of landing and obstacle avoidance in the fruit fly, Drosophila. Journal of Experimental Biology 215: 1783-98.
61. Bender JA, Dickinson MH, (2006) A comparison of visual and haltere-mediated feedback in the control of body saccades in Drosophila melanogaster. Journal of Experimental Biology 209: 4597-4606 doi:10.1242/jeb.02583.
62. Stephens GJ, Bueno de Mesquita M, Ryu WS, Bialek W, (2011) Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 108: 7286-9 doi:10.1073/pnas.1007868108.
63. Geurten BRH, Kern R, Braun E, Egelhaaf M, (2010) A syntax of hoverfly flight prototypes. Journal of Experimental Biology 213: 2461-2475 doi:10.1242/jeb.036079.
64. Rosner R, Egelhaaf M, Grewe J, Warzecha AK, (2009) Variability of blowfly head optomotor responses. Journal of Experimental Biology 212: 1170-1184 doi:10.1242/jeb.027060.
65. Boeddeker N, Dittmar L, Stürzl W, Egelhaaf M, (2010) The fine structure of honeybee head and body yaw movements in a homing task. Proceedings Biological sciences/The Royal Society 277: 1899-906 doi:10.1098/rspb.2009.2326.
66. Bender JA, Dickinson MH, (2006) Visual stimulation of saccades in magnetically tethered Drosophila. The Journal of experimental biology 209: 3170-82 doi:10.1242/jeb.02369.
67. Serres JR, Masson GP, Ruffier F, Franceschini N, (2008) A bee in the corridor: centering and wall-following. Naturwissenschaften 95: 1181-1187 doi:10.1007/s00114-008-0440-6.
68. Tammero LF, Frye MA, Dickinson MH, (2004) Spatial organization of visuomotor reflexes in Drosophila. J Exp Biol 207: 113-122 doi:10.1242/jeb.00724.
69. Pillow JW, Simoncelli EP, (2006) Dimensionality reduction in neural models: an information-theoretic generalization of spike-triggered average and covariance analysis. Journal of vision 6: 414-28 doi:10.1167/6.4.9.
70. Gomez-Marin A, Stephens GJ, Louis M, (2011) Active sampling and decision making in Drosophila chemotaxis. Nature communications 2: 441 doi:10.1038/ncomms1455.
71. Tenenbaum JB, Silva VD, Langford JC, (2000) A Global Geometric Framework for Nonlinear Dimensionality Reduction. Science 290: 2319-2323.
72. Chow DM, Frye MA, (2009) The neuro-ecology of resource localization in Drosophila: Behavioral components of perception and search. Fly 3: 50-61 doi:10.4161/fly.3.1.7775.
73. Krishnan P, Duistermars BJ, Frye MA, (2011) Odor identity influences tracking of temporally patterned plumes in Drosophila. BMC Neuroscience 12: 62 doi:10.1186/1471-2202-12-62.
74. Frye M, Duistermars B, (2009) Visually Mediated Odor Tracking During Flight in Drosophila. Journal of Visualized Experiments Jan 26: 1110.
75. Budick SA, Dickinson MH, (2006) Free-flight responses of Drosophila melanogaster to attractive odors. Journal of Experimental Biology 209: 3001-3017 doi:10.1242/jeb.02305.
76. Iyengar BG, Chou CJ, Vandamme KM, Klose MK, Zhao X, et al. (2011) Silencing synaptic communication between random interneurons during Drosophila larval locomotion. Genes, brain, and behavior 10: 883-900 doi:10.1111/j.1601-183X.2011.00729.x.
77. Katsov AY, Clandinin TR, (2008) Motion processing streams in Drosophila are behaviorally specialized. Neuron 59: 322-35 doi:10.1016/j.neuron.2008.05.022.
78. Stirman JN, Crane MM, Husson SJ, Wabnig S, Schultheis C, et al. (2011) Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nature methods 8: 153-8 doi:10.1038/nmeth.1555.
79. Leifer AM, Fang-Yen C, Gershow M, Alkema MJ, Samuel ADT, (2011) Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nature Methods 8: 147-52 doi:10.1038/nmeth.1554.
80. Naumann EA, Kampff AR, Prober DA, Schier AF, Engert F, (2010) Monitoring neural activity with bioluminescence during natural behavior. Nature neuroscience 13: 513-20 doi:10.1038/nn.2518.
81. Maimon G, Straw AD, Dickinson MH, (2010) Active flight increases the gain of visual motion processing in Drosophila. Nat Neurosci 13: 393-399 doi:10.1038/nn.2492.
82. Seelig JD, Chiappe ME, Lott GK, Dutta A, Osborne JE, et al. (2010) Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nature methods 7: 535-40 doi:10.1038/nmeth.1468.
83. Chiappe ME, Seelig JD, Reiser MB, Jayaraman V, (2010) Walking Modulates Speed Sensitivity in Drosophila Motion Vision. Current Biology 20: 1470-1475 doi:10.1016/j.cub.2010.06.072.