Visual motion-detection circuits in flies: Small-field retinotopic elements responding to motion are evolutionarily conserved across taxa

Journal of Neuroscience

Volumn 16, Issue 15, 1996, Pages 4563-4578

  Buschbeck, Elke K ^a,b   Strausfeld, Nicholas J ^b  

^a University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Diptera; elementary motion detection; evolution; Golgi method; insect vision; neuroanatomy

Indexed keywords

ARTICLE; DENDRITE; EVOLUTION; FLY; GOLGI STAIN; INSECT; MOVEMENT PERCEPTION; NEUROANATOMY; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; VISUAL ILLUSION; VISUAL SYSTEM;

EID: 0029953645     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-15-04563.1996     Document Type: Article

References (78)

1. Bausenwein B, Fischbach K-F (1992a) Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res 270:25-35.
2. Bausenwein B, Fischbach K-F (1992b) 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 (Singh RN, ed), pp 223-239. New Delhi, India: Wiley Eastern.
3. Bodian D (1937) A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat Rec 69:153-162.
4. Boschek CB (1971) On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Z Zellforsch Mikrosk Anat 118:369-409.
5. Braitenberg V (1967) Patterns and projections in the visual system of the fly. I. Retina-lamina projections. Exp Brain Res 3:271-298.
6. Braitenberg V, Hauser-Hohlschuh H (1972) Patterns of projections in the visual system of the fly. II. Quantitative aspects of second order neurons in relation to models of movement perception. Exp Brain Res 16:184-209.
7. Buchner E, Buchner S, Bülthoff I (1984) Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. I. Wild type. J Comp Physiol [A] 155:471-483.
8. Buschbeck E, Strausfeld NJ (1993) Functional aspects of neuroanatomical variation in the dipteran optomotor pathway and the usage of neural characters as a basis for phylogeny inference. In: Proceedings of the 22nd Göttingen Neurobiology Conference (Elsner N, Beer H, eds), p 200. Stuttgart: Thieme.
9. Campos-Ortega JA, Strausfeld NJ (1972) Columns and layers in the second synaptic region of the fly's visual system: the case for two superimposed neuronal architectures. In: Information processing in the visual systems of arthropods (Wehner R, ed), pp 31-36. Berlin: Springer.
10. Campos-Ortega JA, Strausfeld NJ (1973) Synaptic connections of intrinsic cells and basket arborisations in the external plexiform layer of the fly's eye. Brain Res 59:119-136.
11. Collett TS, Land MF (1975) Visual control of flight behaviour in the hoverfly, Syritta pipiens L. J Comp Physiol [A] 99:1-66.
12. Cumming JM, Sinclair BJ, Wood DM (1995) Homology and phylogenetic implications of male genitalia in Diptera-Eremoneura. Entomol Scand 26:121-151.
13. DeVoe RD, Kaiser W, Ohm J, Stone LS (1982) Horizontal movement detectors of honeybees: directionally selective visual neurons in the lobula and brain. J Comp Physiol 147:155-170.
14. Douglass JK, Strausfeld NJ (1995) Visual motion-detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons. J Neurosci 15:5596-5611.
15. Douglass JK, Strausfeld NJ (1996) Visual motion-detection circuits in flies: parallel direction- and nondirection-sensitive pathways between the medulla and lobula plate. J Neurosci, in press.
16. Fischbach K-F, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441-475.
17. Franceschini N (1975) Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In: Photoreceptor optics (Snyder AW, Menzel R, eds), pp 98-125. Berlin: Springer.
18. Franceschini N, Riehle A, Le Nestour A (1989) Directionally selective motion detection by insect neurons. In: Facets of vision (Stavenga DG, Hardie RC, eds), pp 360-390. Berlin: Springer.
19. Frye MA, Olberg RM (1995) Visual receptive field properties of feature-detecting neurons in the dragonfly. J Comp Physiol [B] 177:569-578.
20. Gilbert C, Strausfeld NJ (1992) Small-field neurons associated with oculomotor and optomotor control in muscoid flies: functional organization. J Comp Neurol 316:72-86.
21. Gregory GE (1980) The Bodian Protargol technique. In: Neuroanatomical techniques (Strausfeld NJ, Miller TA, eds), pp 75-95. New York: Springer.
22. Gronenberg W, Strausfeld NJ (1990) Descending neurons supplying the neck and flight motor of Diptera: physiological and anatomical characteristics. J Comp Neurol 302:973-991.
23. Gronenberg W, Strausfeld NJ (1991) Descending pathways connecting the male-specific visual system of flies to the neck and flight motor. J Comp Physiol [A] 169:413-426.
24. Gronenberg W, Strausfeld NJ (1992) Premotor descending neurons responding selectively to local visual stimuli in flies. J Comp Neurol 316:87-103.
25. Hardie RC (1979) Electrophysiological analysis of fly retina I: Comparative properties of R1-6 and R7 and 8. J Comp Physiol 129:19-33.
26. Hardie RC (1983) Projection and connectivity of sex-specific photoreceptors in the compound eye of the male housefly Musca domestica. Cell Tissue Res 233:1-21.
27. Hassenstein B, Reichardt W (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegung-sperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch 11B:513-524.
28. Hausen K, Egelhaaf M (1989) Neural mechanisms of visual course control in insects. In: Facets of vision (Stavenga DG, Hardie RC, eds), pp 391-424. Heidelberg: Springer.
29. Hengstenberg R (1982) Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora erythrocephala. J Comp Physiol [A] 149:179-193.
30. Hennig W (1981) Insect phylogeny. New York: Wiley.
31. Hensler K (1992) Neuronal co-processing of course deviations and head movements in locusts. I. Descending deviation detectors. J Comp Physiol [A] 171:257-272.
32. Järvilehto M, Zettler F (1973) Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina. Z Zellforsch Mikrosk Anat 136:291-306.
33. Kirschfeld K (1967) Die Projecktion der optischen Umwelt auf das Raster der Rhabdomeren im Komplexauge von Musca. Exp Brain Res 3:248-270.
34. Kirschfeld K, Wenk P (1976) The dorsal compound eye of simuliid flies. Z Naturforch 31C:764-765.
35. Kovalev VG (1981) The oldest representatives of the Diptera with short antennae from the Jurassic in Siberia. Paleontol J 15:84-100.
36. Land MF (1993a) The visual control of courtship behavior in the fly Poecilobothrus nobilitatus. J Comp Physiol [A] 173:595-603.
37. Land MF (1993b) Chasing and pursuit in the dolichopodid fly Poecilobothrus nobilitatus. J Comp Physiol [A] 173:605-613.
38. Laughlin SB (1984) The roles of parallel channels in early visual processing by the arthropod compound eye, In: Photoreception and vision in invertebrates (Ali MA, ed), pp 457-481. New York: Plenum.
39. Laughlin SB, Weckström M (1995) Fast and slow receptors - a comparative study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol [A] 172:593-609.
40. McAlpine JF (1989) Phylogeny and classification of the Muscomorpha. In: Manual of nearctic Diptera, Vol 13, Agriculture Canasa Monograph 32 (McAlpine JF, ed), pp 1397-1518.
41. Meinertzhagen IA, Shaw SR (1989) Evolution of synaptic connections between homologous neurons in insects: new cells for old in the optic lobe. In: Neural mechanisms of behavior (Erber J, Menzel R, Pflüger H-J, Todt D, eds), pp 124-126. Stuttgart: G Thieme Verlag.
42. Melzer RR, Paulus HF (1993) Neuroanatomische Studien am Sehsystem von Mücken (Diptera, Nematocera): ein Beitrag zur vergleichenden Analyse neuronaler Strukturen. Verh Dtsch Zool Ges 86:221.
43. Meyer E, Manute C, Streit P, Nässei DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207-216.
44. Olberg RM (1981) Object and self-movement detectors in the ventral nerve cord of the dragonfly. J Comp Physiol [A] 141:327-334.
45. Olberg RM (1986) Identified target-selective visual interneurons descending from the dragonfly brain. J Comp Physiol [A] 159:827-840.
46. Ramon y Cajal S (1937) Recollections of my life (Recuerdos de mi vida), translated by Home Craigie E, Cano J. Cambridge, MA: MIT.
47. Ramon y Cajal S, Sanchez D (1915) Contribucion al conocimiento de los centras nerviosos de los insectos. I. Retina y centras opticos. Trab Lab Invest Biol Univ Madrid 13:1-168.
48. Rind FC (1983) A directionally selective motion detecting neuron in the brain of a moth. J Exp Biol 102:153-171.
49. Shaw SR (1989) The retina lamina pathway in insects, particularly Diptera, viewed from an evolutionary perspective. In: Facets of vision (Stavenga DG, Hardie RC, eds), pp 187-212. Berlin: Springer.
50. Shaw SR (1990) The photoreceptor axon projection and its evolution in the neural superposition eyes of some primitive brachyceran Diptera. Brain Behav Evol 35:107-125.
51. Shaw SR, Meinertzhagen IA (1986) Evolutionary progression at synaptic connections made by identified homologous neurons. Proc Natl Acad Sci USA 83:7961-7965.
52. Shaw SR, Moore D (1989) Evolutionary remodeling in a visual system through extensive changes in the synaptic connectivity of homologous neurones. Vis Neurosci 3:405-410.
53. Shaw SR, Fröhlich A, Meinertzhagen IA (1989) Direct connections between the R7/8 and R1-6 subsystem in the dipteran visual system. Cell Tissue Res 257:295-302.
54. Sinclair BJ, Cumming JM, Wood DM (1993) Homology and phylogenetic implications of male genitalia in Diptera-Lower Brachycera. Entomol Scand 24:407-432.
55. Strausfeld NJ (1970) Golgi studies on insects. II. The optic lobes of Diptera. Philos Trans R Soc Lond [Biol] 258:175-223.
56. Strausfeld NJ (1971) The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurones in the lamina ganglionaris of Diptera. Z Zellforsch Mikrosk Anat 121:377-441.
57. Strausfeld NJ (1976) Atlas of an insect brain. Heidelberg: Springer.
58. Strausfeld NJ (1980) The Golgi method: its application to the insects nervous system and the phenomenon of stochastic impregnation, In: Neuroanatomical techniques (Strausfeld NJ, Miller TA, eds), pp 131-203. New York: Springer.
59. Strausfeld NJ (1996) Oculomotor control in flies: from muscles to elementary motion detectors. In: Neurons, networks, and motor behavior (Stein P, Stuart D, Grillner S, Selverston A, eds), Boston: MIT, in press.
60. Strausfeld NJ, Bassemir UK (1985) Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropil in Calliphora. Cell Tissue Res 240:16-40.
61. Strausfeld NJ, Blest AD (1970) Golgi studies on insects. I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond [Biol] 258:81-174.
62. Strausfeld NJ, Braitenberg V (1970) The compound eye of the fly (Musca domestica): connections between the cartridges of the lamina ganglionaris. Z Vgl Physiol 70:95-104.
63. Strausfeld NJ, Campos-Ortega JA (1973) The L4 monopolar neuron: a substrate for lateral interaction in the visual system of the fly, Musca domestica. Brain Res 59:97-117.
64. Strausfeld NJ, Campos-Ortega JA (1977) Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195:894-897.
65. Strausfeld NJ, Lee JK (1991) Neuronal basis for parallel visual processing in the fly. Vis Neurosci 7:13-33.
66. Strausfeld NJ, Nässei DR (1980) Neuroarchitectures of brain regions that subserve the compound eyes of Crustacea and insects. In: Handbook of sensory physiology. Vol VII/6B, Comparative physiology and evolution of vision in invertebrates (Autrum H, ed), pp 1-132. Berlin: Springer.
67. Torre V, Poggio T (1978) A synaptic mechanism possibly underlying directional selectivity to motion. Proc R Soc Lond [Biol] 202:409-416.
68. Tricca G, Trujillo-Cenóz O (1980) The sexual behavior of the robber-fly Mallophora ruficauda Wied (Asilidae, Asilinae) in normal and experimental conditions. Physiol Behav 25:627-632.
69. Trujillo-Cenóz O, Bernard GD (1972) Some aspects of the retinal organization of Sympycnus lineatus Loew (Diptera, Dolichopodidae). J Ultrastruct Res 38:149-160.
70. Watson ADH, Hardt M (1996) Distribution of synapses on two local auditory interneurons ON1 and ON2 in the prothoracic ganglion of the cricket: relationships with GABA-immunoreactive neurons. Cell Tissue Res 283:231-246.
71. Wicklein M (1993) Motion-sensitive interneurons in the lobula plate of Macroglossum stellatarum. In: Gene-brain-behavior (Elsner N, Heisenberg M, eds), p 366. Proceedings of the 21st Göttingen Neurobiology Conference. Stuttgart: Thieme.
72. Wood DM, Borkent A (1989) Phylogeny and classification of the Nematocera. In: Manual of nearctic Diptera, Sec 13, Agriculture Canasa Monograph 32 (McAlpine JF, ed), pp 1333-1370.
73. Woodly NE (1989) Phylogeny and classification of the "Orthorrhaphous" Brachycera. In: Manual of nearctic Diptera, Sec 13, Agriculture Canasa Monograph 32 (McAlpine JF, ed), pp 1371-1395.
74. Zeil J (1979) A new kind of neural superposition eye: the compound eye of male Bibionidae. Nature 278:240-250.
75. Zeil J (1983a) Sexual dimorphism in the visual system of flies: the compound eye and neural superposition in Bibionidae (Diptera). J Comp Physiol [A] 150:379-393.
76. Zeil J (1983b) Sexual dimorphism in the visual system of flies: the divided brain of male Bibionidae (Diptera). Cell Tissue Res 229:591-610.
77. Zeil J (1983c) Sexual dimorphism in the visual system of flies: the free flight behavior of male Bibionidae (Diptera). J Comp Physiol 150:395-412.
78. Zeil J (1986) The territorial flight of male houseflies (Fannia canicularis L). Behav Ecol Sociobiol 19:213-219.