The computational basis of an identified neuronal circuit for elementary motion detection in dipterous insects

Visual Neuroscience

Volumn 21, Issue 4, 2004, Pages 567-586

  Higgins, Charles M ^a,b   Douglass, John K ^a   Strausfeld, Nicholas J ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

Author keywords

Directional selectivity; Elementary motion detection; Insects; Lobula plate tangential cells; Visual motion

Indexed keywords

4 AMINOBUTYRIC ACID;

ARTICLE; ELECTROPHYSIOLOGY; FLY; IMMUNOREACTIVITY; INTERNEURON; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; NERVE CELL; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA NERVE CELL; STIMULATION; T LYMPHOCYTE; VISUOMOTOR COORDINATION;

ANIMALS; DIPTERA; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NERVOUS SYSTEM PHYSIOLOGY; NEURAL PATHWAYS; NEURONS, AFFERENT; PHOTIC STIMULATION; PHOTORECEPTORS; RETINA;

EID: 10644223122     PISSN: 09525238     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0952523804214079     Document Type: Article

References (57)

1. ADELSON, E.H. & BERGEN, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 2(2), 284-299.
2. BARLOW, H.B. & LEVICK, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology (London) 178, 477-504.
3. BAUSENWEIN, B. AND FISCHBACH, K.-F. (1992). Separation of functional pathways in the fly's medulla: combination of 2-deoxyglucose studies with anatomical fine analysis. In Nervous Systems: Principles of Design and Function, ed. SINGH, R.N., pp. 223-239. New Delhi, India: Wiley Eastern.
4. BORST, A. (2001). Modelling fly motion vision. In Computational Neuroscience: A Comprehensive Approach, ed. FENG, JIANFENG, pp. 401-434. Boca Raton, FL: CRC Press.
5. BORST, A. AND HAAG, J. (2002). Neural networks in the cockpit of the fly. Journal of Comparative Physiology A 188, 419-437.
6. BOSCHEK, C.B. (1971). On the fine structure of the peripheral retina and the lamina of the fly, Musca domestica. Zeitschrift für Zellforschung und Mikroskopische Anatomie 110, 336-349.
7. BUCHNER, E. & BUCHNER, S. (1984). Neuroanatomical mapping of visually induced neuron activity in insects by 3H-deoxyglucose. In Photoreception and Vision in Invertebrates, ed. ALI, M.A., pp. 623-634. New York: Plenum Press.
8. BUCHNER, E., BUCHNER, S., & HENGSTENBERG, R. (1979). 2-Deoxy-D-glucose maps movement-specific nervous activity in the second visual ganglion of Drosophila. Science 205, 687-688.
9. BUSCHBECK, E.K. & STRAUSFELD, N.J. (1996). Visual motion-detection circuits in flies: Small field retinotopic elements responding to motion are evolutionarily conserved across taxa. Journal of Neuroscience 16, 4563-4578.
10. CAMPOS-ORTEGA, J.A. & STRAUSFELD, N.J. (1973). Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly's eye. Brain Research 59, 119-136.
11. CLIFFORD, C.W.G. & IBBOTSON, M.R. (2003). Fundamental mechanisms of visual motion detection: Models, cells and functions. Progress in Neurobiology 68, 409-437.
12. COLLETT, T.S. & LAND, M.F. (1978). How hoverflies compute interception courses. Journal of Comparative Physiology 125, 191-204.
13. COOMBE, P.E., SRINIVASAN, M.V., & GUY, R.G. (1989). Are the large monopolar cells of the insect lamina on the optomotor pathway? Journal of Comparative Physiology A 166, 23-35.
14. DE RUYTER VAN STEVENINCK, R., LEWEN, G.D., STRONG, S.P., KOBERLE, R., & BIALEK, W. (1997). Reproducibility and variability in neural spike trains. Science 275, 1805-1808.
15. DOUGLASS, J.K. & STRAUSFELD, N.J. (1995). Visual motion detection circuits in flies: Peripheral motion computation by identified small field retinotopic neurons. Journal of Neuroscience 15, 5596-5611.
16. DOUGLASS, J.K. & STRAUSFELD, N.J. (1996). Visual motion detection circuits in flies: Parallel direction-and non-direction sensitive pathways between the medulla and lobula plate. Journal of Neuroscience 16, 4551-4562.
17. DOUGLASS, J.K. & STRAUSFELD, N.J. (1998). Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly. Journal of Comparative Neurology 396: 84-104.
18. DOUGLASS, J.K. & STRAUSFELD, N.J. (2004). Sign-conserving amacrines in the fly's external plexiform layer. Visual Neuroscience (in review).
19. DVORAK, D.R., BISHOP, L.G., & ECKERT, H.E. (1975). Intracellular recording and staining of directionally selective motion detecting neurons in fly optic lobe. Vision Research 15, 451-453.
20. EGELHAAF, M. & BORST, A. (1989). Transient and steady-state response properties of movement detectors. Journal of the Optical Society of America A 6, 116-127.
21. EGELHAAF, M., BORST, A., & REICHARDT, W. (1989). Computational structure of a biological motion-detection system as revealed by local detector analysis in the fly's nervous system. Journal of the Optical Society of America A 6, 1070-1087.
22. EGELHAAF, M., BORST, A., WARZECHA, A.K., FLECKS, S., & WILDEMANN, A. (1993). Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques. Journal of Neurophysiology 69, 340-351.
23. EGELHAAF, M., HAUSEN, K., REICHARDT, W., & WEHRHAHN, C. (1988). Visual course control in flies relies on neuronal computation of object and background motion. Trends in Neuroscience 11, 351-358.
24. FISCHBACH, K.-F. & DITTRICH, A.P.M. (1989). The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell and Tissue Research 258, 441-475.
25. FRANCESCHINI, N., PUEHLE, A., & LE NESTOUR, A. (1989). Directionally selective motion detection by insect neurons. In Facets of Vision, ed. STAVENGA, D.G. & HARDIE, R.C., chapter 17, pp. 360-390. Springer-Verlag.
26. FRIED, S.I., MÜNCH, T.A., & WERBLIN, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411-414.
27. GILBERT, C. & STRAUSFELD, N.J. (1991). The functional organization of male-specific visual neurons in flies. Journal of Comparative Physiology A 169, 395-411.
28. HARRIS, R.A., O'CARROLL, D.C., & LAUGHLIN, S.B. (1999). Adaptation and the temporal delay filter of fly motion detectors. Vision Research 39, 2603-2613.
29. HASSENSTEIN, B. (1950). Wandernde geometrische Interferenzfiguren im Insektenauge. Naturwissenschaften 37, 45-46.
30. HASSENSTEIN, B. (1951). Ommatidienraster und afferente Bewegungsintegration. Zeitschrift für vergleichende Physiologie 33, 301-326.
31. HASSENSTEIN, B. (1958). Die Stärke von optokinetschen Reaktionen auf verschiedene Mustergeschwindigkeiten. Zeitschrift für Naturforschung 13b, 1-6.
32. HASSENSTEIN, B. & REICHARDT, W. (1956). Systemtheorische analyse der Zeit-, Reihenfolgen-und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Zeitschrift für Naturforschung 11b, 513-524.
33. HAUSEN, K. (1982). Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: Structure and signals. Biological Cybernetics 45, 143-156.
34. HAUSEN, K. (1984). The lobula-complex of the fly: Structure, function, and significance in visual behaviour. In Photoreception and Vision in Invertebrates, ed. ALI, M.A., pp. 523-599. New York: Plenum Press.
35. HILDRETH, E.C. & KOCH, C. (1987). The analysis of visual-motion-from computational theory to neuronal mechanisms. Annual Review of Neuroscience 10, 477-533.
36. IBBOTSON, M.R. (2001). Identification of mechanisms underlying motion detection in mammals. In Motion Vision: Computational, Neural, and Ecological Constraints, ed. ZANKER, J.M. & ZEIL, J., pp. 57-65. Berlin: Springer.
37. JAMES, A.C. & OSORIO, D. (1996). Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques. Journal of Comparative Physiology A 178, 183-199.
38. JÄRVILEHTO, M. & ZETTLER, F. (1973). Electrophysiological- histological studies on some functional properties of visual cells and second-order neurons of an insect retina. Zeitshchrift für Zellforschung und Mikroskopische Anatomie 136, 291-306.
39. KOCH, C. (1999). Biophysics of Computation: Information Processing in Single Neurons. New York: Oxford University Press.
40. KOCH, C., POGGIO, T., & TORRE, V. (1982). Retinal ganglion cells: A functional interpretation of dendritic morphology. Philosophical Transactions of the Royal Society B (London) 298, 227-264.
41. KRAPP, H.G., HENGSTENBERG, B., & HENGSTENBERG, R. (1998). Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. Journal of Neurophysiology 79, 1902-1917.
42. LAUGHLIN, S. (1984). The roles of parallel channels in early visual processing by the arthropod compound eye. In Photoreception and Vision in Invertebrates, ed. ALI, M.A., pp. 457-482. New York: Plenum Press.
43. MADDESS, T. & LAUGHLIN, S.B. (1985). Adaptation of the motion sensitive neuron H1 is generated locally and governed by contrast frequency. Proceedings of the Royal Society B (London) 225, 251-275.
44. NILSSON, D.-E. (1989). Optics and evolution of the compound eye. In Facets of Vision, ed. STAVENGA, D.G. & HARDIE, R.C., Chapter 3, pp. 30-73. Berlin: Springer-Verlag.
45. O'CARROLL, D.C. (2001). Motion adaptation and evidence for parallel processing in the lobula plate of the bee-fly Bombylius major. In Motion Vision: Computational, Neural, and Ecological Constraints, ed. ZANKER, J.M. & ZEIL, J., pp. 381-394. Berlin: Springer.
46. PIX, W., ZANKER, J.M., & ZEIL, J. (2000). The optomotor response and spatial resolution of the visual system in male Xenos vesparum (strepsiptera). Journal of Experimental Biology 203, 3397-3409.
47. REICHARDT, W., EGELHAAF, M., & GUO, A.K. (1989). Processing of figure and background motion in the visual-system of the fly. Biological Cybernetics 61, 327-345.
48. RIVERA-ALVIDREZ, Z. & HIGGINS, C.M. (2004). Contrast saturation in a neuronally-based model of elementary motion detection. Neurocomputing. (In Press)
49. SINAKEVITCH, I. & STRAUSFELD, N.J. (2004). Chemical neuroanatomy of the fly's movement detection pathway. Journal of Comparative Neurology 486, 6-23.
50. STAVENGA, D.G. (1979). Pseudopupils of compound eyes. In Handbook of Sensory Physiology, ed. AUTRUM, H., Vol. VII/6A, chapter 7, pp. 357-439. Berlin: Springer.
51. STERLING, P. (2002). How neurons compute direction. Nature 420, 375-376.
52. STRAUSFELD, N.J. (1976). Atlas of an insect brain. Heidelberg, New York: Springer.
53. STRAUSFELD, N.J. & CAMPOS-ORTEGA, J.A. (1977). Vision in insects: Pathways possibly underlying neural adaptation and lateral inhibition. Science 195, 894-897.
54. STRAUSFELD, N.J. & LEE, J.K. (1991). Neuronal basis for parallel visual processing in the fly. Visual Neuroscience 7, 13-33.
55. TORRE, V. & POGGIO, T. (1978). Synaptic mechanism possibly underlying directional selectivity to motion. Proceedings of the Royal Society B (London) 202, 409-416.
56. VAN SANTEN, J.P.H. & SPERLING, G. (1985). Elaborated Reichardt detectors. Journal of the Optical Society of America A 2, 300-320.
57. WICKLEIN, M. & STRAUSFELD, N.J. (2000). The organization and significance of neurons detecting change of depth in the hawk moth Manduca sexta. Journal of Comparative Neurology 424(2), 356-376.