Contributions of the 12 Neuron Classes in the Fly Lamina to Motion Vision

Neuron

Volumn 79, Issue 1, 2013, Pages 128-140

  Tuthill, JohnC ^a,b   Nern, Aljoscha ^a,b   Holtz, StephenL ^a   Rubin, GeraldM ^a   Reiser, MichaelB ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA; FEMALE; LAMINA NEURON; MOVEMENT PERCEPTION; NEUROMODULATION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PSYCHOPHYSICS; SPINAL CORD NERVE CELL; VISUAL STIMULATION; VISUAL SYSTEM;

ANIMALS; DROSOPHILA; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NEURONS; PHOTORECEPTOR CELLS, INVERTEBRATE; VISUAL PATHWAYS;

EID: 84880008959     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.05.024     Document Type: Article

References (76)

1. Anstis S.M., Rogers B.J. Illusory reversal of visual depth and movement during changes of contrast. Vision Res. 1975, 15:957-961.
2. Baines R.A., Uhler J.P., Thompson A., Sweeney S.T., Bate M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J.Neurosci. 2001, 21:1523-1531.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B-Methodol. 1995, 57:289-300.
4. Borst A., Euler T. Seeing things in motion: models, circuits, and mechanisms. Neuron 2011, 71:974-994.
5. Borst A., Haag J., Reiff D.F. Fly motion vision. Annu. Rev. Neurosci. 2010, 33:49-70.
6. Braitenberg V. Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Exp. Brain Res. 1967, 3:271-298.
7. Braitenberg V., Debbage P. A regular net of reciprocal synapses in the visual system of the fly, Musca domestica. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1974, 90:25-31.
8. Buchner, E. (1971). Dunkelanregung des stationären Flugs der Fruchtfliege Drosophila. PhD thesis, Univeristy of Tübingen, Tübingen, Germany.
9. Buchner E. Elementary movement detectors in an insect visual system. Biol. Cybern. 1976, 24:85-101.
10. Buchner E. Behavioural analysis of spatial vision in insects. Photoreception and Vision in Invertebrates 1984, 561-619. Plenum, New York. M. Ali (Ed.).
11. Carver S., Roth E., Cowan N.J., Fortune E.S. Synaptic plasticity can produce and enhance direction selectivity. PLoS Comput. Biol. 2008, 4:e32.
12. Cavanagh P., Anstis S. The contribution of color to motion in normal and color-deficient observers. Vision Res. 1991, 31:2109-2148.
13. Chichilnisky E.J., Heeger D., Wandell B.A. Functional segregation of color and motion perception examined in motion nulling. Vision Res. 1993, 33:2113-2125.
14. Clark D.A., Bursztyn L., Horowitz M.A., Schnitzer M.J., Clandinin T.R. Defining the computational structure of the motion detector in Drosophila. Neuron 2011, 70:1165-1177.
15. Coombe P.E., Srinivasan M.V., Guy R.G. Are the large monopolar cells of the insect lamina on the optomotor pathway?. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1989, 166:23-35.
16. Csete M.E., Doyle J.C. Reverse engineering of biological complexity. Science 2002, 295:1664-1669.
17. Douglass J.K., Strausfeld N.J. Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons. J.Neurosci. 1995, 15:5596-5611.
18. Duistermars B.J., Chow D.M., Condro M., Frye M.A. The spatial, temporal and contrast properties of expansion and rotation flight optomotor responses in Drosophila. J.Exp. Biol. 2007, 210:3218-3227.
19. Duistermars B.J., Reiser M.B., Zhu Y., Frye M.A. Dynamic properties of large-field and small-field optomotor flight responses in Drosophila. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2007, 193:787-799.
20. Duistermars B.J., Care R.A., Frye M.A. Binocular interactions underlying the classic optomotor responses of flying flies. Front. Behav. Neurosci. 2012, 6:6.
21. Egelhaaf M., Borst A. Transient and steady-state response properties of movement detectors. J.Opt. Soc. Am. A 1989, 6:116-127.
22. Eichner H., Joesch M., Schnell B., Reiff D.F., Borst A. Internal structure of the fly elementary motion detector. Neuron 2011, 70:1155-1164.
23. Farrow K., Haag J., Borst A. Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron. Nat. Neurosci. 2006, 9:1312-1320.
24. Fei H., Chow D.M., Chen A., Romero-Calderón R., Ong W.S., Ackerson L.C., Maidment N.T., Simpson J.H., Frye M.A., Krantz D.E. Mutation of the Drosophila vesicular GABA transporter disrupts visual figure detection. J.Exp. Biol. 2010, 213:1717-1730.
25. Fischbach K.F., Dittrich A.P. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 1989, 258:441-475.
26. Gao S., Takemura S.Y., Ting C.Y., Huang S., Lu Z., Luan H., Rister J., Thum A.S., Yang M., Hong S.T., et al. The neural substrate of spectral preference in Drosophila. Neuron 2008, 60:328-342.
27. Gollisch T., Meister M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 2010, 65:150-164.
28. Götz K.G. Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik 1964, 2:77-92.
29. Götz K.G. Flight control in Drosophila by visual perception of motion. Kybernetik 1968, 4:199-208.
30. Götz K.G. Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J.Exp. Biol. 1987, 128:35-46.
31. Haag J., Denk W., Borst A. Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. Proc. Natl. Acad. Sci. USA 2004, 101:16333-16338.
32. Hamada F.N., Rosenzweig M., Kang K., Pulver S.R., Ghezzi A., Jegla T.J., Garrity P.A. An internal thermal sensor controlling temperature preference in Drosophila. Nature 2008, 454:217-220.
33. Hardie R.C., Weckström M. Three classes of potassium channels in large monopolar cells of the blowfly Calliphora vicina. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1990, 167:723-736.
34. Hasegawa E., Kitada Y., Kaido M., Takayama R., Awasaki T., Tabata T., Sato M. Concentric zones, cell migration and neuronal circuits in the Drosophila visual center. Development 2011, 138:983-993.
35. Hassenstein V.B., Reichardt W. Systemtheoretische Analyse der Zeit-, Reihenfolgen und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch 1956, 11b:513-524.
36. Hausen K. Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: receptive-field organization and response characteristics. Biol. Cybern. 1982, 46:67-79.
37. Hausen K., Wehrhahn C. Neural circuits mediating visual flight control in flies. I. Quantitative comparison of neural and behavioral response characteristics. J.Neurosci. 1989, 9:3828-3836.
38. Heisenberg M. Comparative behavioral studies on 2 visual mutants of Drosophila. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1972, 80:119-136.
39. Heisenberg M., Wolf R. Vision in Drosophila: Genetics of Microbehavior 1984, Springer-Verlag, Berlin.
40. Helfrich-Förster C., Shafer O.T., Wülbeck C., Grieshaber E., Rieger D., Taghert P. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J.Comp. Neurol. 2007, 500:47-70.
41. Jenett A., Rubin G.M., Ngo T.T., Shepherd D., Murphy C., Dionne H., Pfeiffer B.D., Cavallaro A., Hall D., Jeter J., et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2012, 2:991-1001.
42. Joesch M., Schnell B., Raghu S.V., Reiff D.F., Borst A. ON and OFF pathways in Drosophila motion vision. Nature 2010, 468:300-304.
43. Joesch M., Weber F., Eichner H., Borst A. Functional specialization of parallel motion detection circuits in the fly. J.Neurosci. 2013, 33:902-905.
44. Katsov A.Y., Clandinin T.R. Motion processing streams in Drosophila are behaviorally specialized. Neuron 2008, 59:322-335.
45. Kirschfeld K. Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von MUSCA. Exp. Brain Res. 1967, 3:248-270.
46. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J.Neurobiol. 2001, 47:81-92.
47. Kolodziejczyk A., Sun X., Meinertzhagen I.A., Nässel D.R. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS ONE 2008, 3:e2110.
48. Krapp H.G., Hengstenberg B., Hengstenberg R. Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J.Neurophysiol. 1998, 79:1902-1917.
49. Krapp H.G., Hengstenberg R., Egelhaaf M. Binocular contributions to optic flow processing in the fly visual system. J.Neurophysiol. 2001, 85:724-734.
50. Laughlin S.B., Hardie R.C. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1978, 128:319-340.
51. Laughlin S.B., Howard J., Blakeslee B. Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proc. R. Soc. Lond. B Biol. Sci. 1987, 231:437-467.
52. Luan H., Peabody N.C., Vinson C.R., White B.H. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 2006, 52:425-436.
53. Meinertzhagen I.A., O'Neil S.D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J.Comp. Neurol. 1991, 305:232-263.
54. Pfeiffer B.D., Jenett A., Hammonds A.S., Ngo T.T., Misra S., Murphy C., Scully A., Carlson J.W., Wan K.H., Laverty T.R., et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 2008, 105:9715-9720.
55. Pfeiffer B.D., Ngo T.T., Hibbard K.L., Murphy C., Jenett A., Truman J.W., Rubin G.M. Refinement of tools for targeted gene expression in Drosophila. Genetics 2010, 186:735-755.
56. Pulver S.R., Pashkovski S.L., Hornstein N.J., Garrity P.A., Griffith L.C. Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J.Neurophysiol. 2009, 101:3075-3088.
57. Reichardt W. Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. Sensory Communication 1961, 303-317. John Wiley, New York. W.A. Rosenblith (Ed.).
58. Reichardt W., Wenking H. Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 1969, 56:424-425.
59. Reiff D.F., Plett J., Mank M., Griesbeck O., Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nat. Neurosci. 2010, 13:973-978.
60. Reiser M.B., Dickinson M.H. A modular display system for insect behavioral neuroscience. J.Neurosci. Methods 2008, 167:127-139.
61. Rister J., Pauls D., Schnell B., Ting C.Y., Lee C.H., Sinakevitch I., Morante J., Strausfeld N.J., Ito K., Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 2007, 56:155-170.
62. Rivera-Alba M., Vitaladevuni S.N., Mishchenko Y., Lu Z., Takemura S.Y., Scheffer L., Meinertzhagen I.A., Chklovskii D.B., de Polavieja G.G. Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. Curr. Biol. 2011, 21:2000-2005.
63. Single S., Borst A. Dendritic integration and its role in computing image velocity. Science 1998, 281:1848-1850.
64. Single S., Haag J., Borst A. Dendritic computation of direction selectivity and gain control in visual interneurons. J.Neurosci. 1997, 17:6023-6030.
65. Smear M.C., Tao H.W., Staub W., Orger M.B., Gosse N.J., Liu Y., Takahashi K., Poo M.M., Baier H. Vesicular glutamate transport at a central synapse limits the acuity of visual perception in zebrafish. Neuron 2007, 53:65-77.
66. Srinivasan M.V., Laughlin S.B., Dubs A. Predictive coding: a fresh view of inhibition in the retina. Proc. R. Soc. Lond. B Biol. Sci. 1982, 216:427-459.
67. Strausfeld N.J., Campos-Ortega J.A. The L4 monopolar neurone: a substrate for lateral interaction in the visual system of the fly Musca domestica (L.). Brain Res. 1973, 59:97-117.
68. Struhl G., Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993, 72:527-540.
69. Takemura S.Y., Lu Z., Meinertzhagen I.A. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J.Comp. Neurol. 2008, 509:493-513.
70. Takemura S.Y., Karuppudurai T., Ting C.Y., Lu Z., Lee C.H., Meinertzhagen I.A. Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr. Biol. 2011, 21:2077-2084.
71. Tammero L.F., Frye M.A., Dickinson M.H. Spatial organization of visuomotor reflexes in Drosophila. J.Exp. Biol. 2004, 207:113-122.
72. Theobald J.C., Ringach D.L., Frye M.A. Dynamics of optomotor responses in Drosophila to perturbations in optic flow. J.Exp. Biol. 2010, 213:1366-1375.
73. Tuthill J.C., Chiappe M.E., Reiser M.B. Neural correlates of illusory motion perception in Drosophila. Proc. Natl. Acad. Sci. USA 2011, 108:9685-9690.
74. Zabala F., Polidoro P., Robie A., Branson K., Perona P., Dickinson M.H. A simple strategy for detecting moving objects during locomotion revealed by animal-robot interactions. Curr. Biol. 2012, 22:1344-1350.
75. Zheng L., de Polavieja G.G., Wolfram V., Asyali M.H., Hardie R.C., Juusola M. Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J.Gen. Physiol. 2006, 127:495-510.
76. Zhu Y., Nern A., Zipursky S.L., Frye M.A. Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr. Biol. 2009, 19:613-619.