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Neuronal basis for parallel visual processing in the fly

Published online by Cambridge University Press:  02 June 2009

Nicholas J. Strausfeld  and
Jong-Kyoo Lee
Nicholas J. Strausfeld
Affiliation:
Division of Neurobiology, Arizona Research Laboratories, University of Arizona, Tueson
Jong-Kyoo Lee
Affiliation:
Division of Neurobiology, Arizona Research Laboratories, University of Arizona, Tueson
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Abstract

Behavioral and electrophysiological studies of insects demonstrate both spectrally independent and chromatically dependent behaviors and interneurons. This account describes the neuroanatomical identification of two parallel retinotopic subsystems, one supplying descending channels to spectrally independent neck and flight motor circuits, the other supplying polychromatic channels to neuropils associated with leg motor circuits in the thoracic ganglia. In the compound eye, two classes of photoreceptors contribute to each of several thousand sampling units. High-sensitivity, chromatically uniform short-axon photoreceptors (R1-R6) supply the lamina's external plexiform layer and are presynaptic to L1, L2 efferents. These project in parallel with a second system of trichromatic long-axon receptors and the L3 efferent. Both pathways supply columns of the medulla, equal in number to ommatidia. Golgi and cobalt-silver impregnation demonstrates that neurons from the medulla diverge to two deeper regions, the lobula plate and lobula, the former a thin tectum of neuropil dorsal to the more substantial lobula. Layer relationships between medulla neurons and their afferent supply suggest that the lobula plate and lobula are each supplied by one or the other, but not both, of the two parallel subsystems. Independence of the two parallel pathways is suggested by ablation of the photoreceptor layer leading to selective degeneration of the motion-sensitive lobula plate neuropil. In addition, octets of small-field neurons associated with the R1-R6/L1, L2 pathway give rise to synaptic complexes with motion-sensitive neurons of the lobula plate. A variety of behavioral and electrophysiological studies provide supporting evidence that certain insects possess parallel visual pathways comparable to the magnocellular and parvocellular subsystems of primates.

Keywords

Parallel pathwaysSpectral independenceColor visionInsectsNeuroanatomy
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 1-2 , August 1991 , pp. 13 - 33
Copyright
Copyright © Cambridge University Press 1991

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References

Anderson, A. (1972). The ability of honey bees to generalize visual stimuli. In Information Processing in the Visual System of Arthropods, ed. Wehner, R., pp. 207–215. Heidelberg, Berlin: Springer Verlag.Google Scholar
Backhaus, W., Menzel, R. & Kreissl, S. (1987a). Multidimensional scaling of color similarity in bees. Biological Cybernetics 55, 331–333.Google Scholar
Backhaus, W., Werner, A. & Menzel, R. (1987b). Color vision in honeybees: metric, dimensions, constancy, and ecological aspects. In Neurobiology and Behavior of the Honeybee, ed. Menzel, R. & Mercer, A. pp. 83–97. Heidelberg, Berlin: Springer Verlag.Google Scholar
Bacon, J.P. & Strausfeld, N.J. (1986). The dipteran ‘Giant fibre’ pathway: neurons and signals. Journal of Comparative Physiology A 158, 529–548.CrossRefGoogle Scholar
Bodian, D. (1937). A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anatomical Record 69, 153–162.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109–184.Google Scholar
Boycott, B.B. & Kolb, H. (1973). The connections between bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 115–140.CrossRefGoogle ScholarPubMed
Braitenberg, V. (1967). Patterns of projection in the visual system of the fly, I: Retina-lamina projections. Experimental Brain Research 3, 271–298.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Cajal, S.R. (1937). Recollections of My Life (Recuerdos De Mi Vida). Translation by Horne, E.C. & Cano, J.Cambridge: MIT Press.Google Scholar
Cajal, S.R. & Sánchez, D.S. (1915). Contribucion al conocimiento de los centros nerviosos de los insectos. Parte I: Retina y centros opticos. Trabajos del Laboratorio de Investigaciones Biologicas de la Universidad de Madrid 13, 1–168.Google Scholar
Campos-Ortega, J.A. & Strausfeld, N.J. (1972). The columnar organization of the second synaptic region of the visual system of Musca domestica L, I: Receptor terminals in the medulla. Zeitschrift für Zellforschung 124, 561–582.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Desclin, J.C. & Escubi, J. (1975). An additional silver-impregnation method for demonstration of degenerating nerve cells and processes in the central nervous system. Brain Research 93, 25–39.CrossRefGoogle ScholarPubMed
Devoe, R.D., Kaiser, W., Ohm, J. & Stone, L.S. (1982). Horizontal movement detectors of honeybees: directionally selective visual neurons in the lobula and brain. Journal of Comparative Physiology A 147, 155–170.CrossRefGoogle Scholar
De Yoe, E.A. & Van Essen, D.R. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 217–226.Google ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B (London) 166, 80–111.Google Scholar
Eckert, H. (1971). Die spektrale Empfindlichkeit des Komplexauges von Musca (Bestimmung aus Messung der optomotorischen Reaktion). Kybernetik 9, 145–150.CrossRefGoogle ScholarPubMed
Egelhaaf, M. (1985a). On the neuronal basis of figure-ground discrimination by relative motion in the fly, I: Behavioral constraints imposed on the neuronal network and the role of the optomotor system. Biological Cybernetics 52, 123–140.CrossRefGoogle Scholar
Egelhaaf, M. (1985b). On the neural basis of figure-ground discrimination by relative motion in the visual system of the fly, II: Figure-detection cells, a new class of visual interneurones. Biological Cybernetics 52, 195–209.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Franceschini, N. (1975). Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 75–82. Berlin, Heidelberg, New York: Springer Verlag.Google Scholar
Franceschini, N., Riehle, A. & Le Nestour, A. (1989). Directionally selective motion detection by insect neurons. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 360–390. Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Fukushi, T. (1990). Learning and discrimination of coloured papers in the walking blowfly (Lucilia coprina). Journal of Comparative Physiology A 166, 57–64.Google Scholar
Fukushi, T. (1989). Colour discrimination from various shades of grey in the trained blowfly (Lucilia coprina). Journal of Insect Physiology 36, 69–75.CrossRefGoogle Scholar
Gilbert, C. & Strausfeld, N.J. (1991) The functional organization of male-specific visual neurons in flies. Journal of Comparative Physiology. 168 (in press).Google Scholar
Glauert, A.M. (1975). Fixation, dehydration, and embedding of biological specimens. In Practical Methods in Electron Microscopy, Vol. 3, ed. Glauert, A.M., pp. 1–207. Amsterdam, Oxford, New York: Elsevier.Google Scholar
Gregory, G.E. (1980). The Bodian protargol technique. In Neuroanatomical Techniques: Insect Nervous System, ed. Strausfeld, N.J., pp. 77–97. Heidelberg, New York: Springer Verlag.Google Scholar
Griffiths, G.W. & Boschek, C.B. (1976). Rapid degeneration of visual fibers following retinal degeneration in the dipteran compound eye. Neuroscience Letters 3, 253–258.CrossRefGoogle ScholarPubMed
Gronenberg, W. & Strausfeld, N.J. (1990). Descending neurons supplying the neck and flight motor of Diptera: physiological and anatomical characteristics. Journal of Comparative Neurology 302, 973–991.CrossRefGoogle ScholarPubMed
Gronenberg, W. & Strausfeld, N.J. (1991) Descending pathways connecting male-specific visual system of flies to the neck and flight motor. Journal of Comparative Physiology 168 (in press).Google Scholar
Hardie, R.C. (1984). Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. Journal of Comparative Physiology 154, 157–165.CrossRefGoogle Scholar
Hardie, R.C. (1988). The photoreceptor array of the dipteran retina. Trends in Neuroscience 9, 419–423.CrossRefGoogle Scholar
Hausen, K. (1976). Functional characterization and anatomical identification of motion-sensitive neurons in the lobula plate of the blowfly (Calliphora erythrocephala). Zeitschrift für Naturforschung 31c, 629–633.CrossRefGoogle Scholar
Hausen, K. (1984). The lobula complex of the fly: structure, function, and significance in visual behavior. In Photoreception and Vision in Invertebrates, ed. Ali, M.A., pp. 523–599. New York: Plenum.CrossRefGoogle Scholar
Hausen, K. & Egelhaaf, M. (1989). Neural mechanisms of visual course control in insects. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 391–424. Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Hausen, K. & Strausfeld, N.J. (1980). Sexually dimorphic interneuron arrangements in the fly visual system. Proceedings of the Royal Society B (London) 208, 57–71.Google Scholar
Hengstenberg, R. (1982). Common visual response properties of giant vertical cells in the lobula plate of the blowfly (Calliphora erythrocephala). Journal of Comparative Physiology A 149, 179–193.CrossRefGoogle Scholar
Hengstenberg, R. (1984). Roll stabilization during flight of the blow fly's head and body by mechanical and visual cues. In Localization and Orientation in Biology and Engineering, ed. Varju, D. & Schnitzler, V., pp. 121–134. Berlin, Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Hertel, H. (1980). Chromatic properties of identified interneurons in the optic lobes of the bee. Journal of Comparative Physiology A 137, 215–232.CrossRefGoogle Scholar
Hertel, H. & Maronde, U. (1987). Processing of visual information in the honey brain. In Neurobiology and Behavior of the Honeybee, ed. Menzel, R. & Mercer, A., pp. 141–151. Heidelberg, Berlin: Springer Verlag.CrossRefGoogle Scholar
Hubel, D. & Livingstone, M. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7, 3378–3415.CrossRefGoogle ScholarPubMed
Ibbotson, M.R. (1991). Wide-field motion-sensitive descending neurons tuned to horizontal movement in the honeybee (Apis mellifera). Journal of Comparative Physiology A 168, 91–102.CrossRefGoogle Scholar
Kaiser, W. (1968). Zur Frage des Unterscheidungsvermögens für Spektralfarben: eine Untersuchung der Optomotrik der königlichen Glanzfliege (Phormia regina Meig). Zeitschrift für vergleichende Physiologie 61, 71–85.CrossRefGoogle Scholar
Kaiser, W. (1975). The relationship between visual movement detection and colour vision in insects. In The Compound Eye and Vision in Insects, ed. Horridge, G.A., pp. 359–371. Oxford: Clarendon Press.Google Scholar
Kaiser, W., Seidle, R. & Vollmar, J. (1977). The participation of all three colour receptors in the phototactic behavior of fixed walking honeybees. Journal of Comparative Physiology A 122, 27–44.CrossRefGoogle Scholar
Kenyon, F.C. (1896). The brain of the bee. Journal of Comparative Neurology 6, 133–210.CrossRefGoogle Scholar
Kirschfeld, K. (1967). Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Experimental Brain Research 3, 248–270.CrossRefGoogle ScholarPubMed
Kirschner, W.H. & Srinivasan, M.V. (1989). Freely flying honeybees use image motion to estimate object distance. Naturwissenschaften 76, 281–282.CrossRefGoogle Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society B (London) 258, 261–283.Google Scholar
Land, M.F. & Collett, T.S. (1974). Chasing behavior of houseflies (Fannia canicularis). Journal of Comparative Physiology A 89, 331–357.CrossRefGoogle Scholar
Land, M.F. & Eckert, H.E. (1985). Maps of the acute zones of fly eyes. Journal of Comparative Physiology A 156, 525–538.CrossRefGoogle Scholar
Laughlin, S.B. (1981). Neural principles in the peripheral visual systems of invertebrates. In Handbook of Sensory Physiology, VII/6B, ed. Autrum, H., pp. 133–280. Heidelberg, New York, Berlin: Springer Verlag.Google Scholar
Lillywhite, P.G. & Dvorak, D. (1981). Responses to single photons in a fly optomotor neurone. Vision Research 21, 279–290.CrossRefGoogle Scholar
Livingstone, M. & Hubel, D. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. Journal of Neuroscience 7, 3416–3468.CrossRefGoogle ScholarPubMed
Livingstone, M. & Hubel, D. (1988). Segregation of form, color movement, and depth: anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
Mazochin-Porshnyakov, G.A. (1969). Die Fähigkeit der Bienen, visuelle Reize zu generalisieren. Zeitschrift für vergleichende Physiology 65, 15–28.CrossRefGoogle Scholar
Meinertzhagen, I.A. & O'Niel, S.D. (1991). The synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. Journal of Comparative Neurology 305, 232–263.CrossRefGoogle ScholarPubMed
Menzel, R. & Backhaus, W. (1989). Color vision in honeybees: phenomena and physiological mechanisms. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 281–297. Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Milde, J.J. & Strausfeld, N.J. (1990). Cluster organization and response characteristics of the giant fiber pathway of the blowfly (Calliphora erythrocephala). Journal of Comparative Neurology 294, 59–75.CrossRefGoogle ScholarPubMed
Milde, J.J., Seyan, H.S. & Strausfeld, N.J. (1987). The neck motor system of the fly (Calliphora erythrocephala), II: Sensory organization. Journal of Comparative Physiology A 160, 225–238.CrossRefGoogle Scholar
Millonig, G. (1961). Advantages of a phosphate buffer for OsO4 solutions in fixation. Journal of Applied Physiology 32, 1637.Google Scholar
Nilsson, D.-E. (1987). Optics and evolution of the compound eye. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 30–73. Heidelberg, New York: Springer Verlag.Google Scholar
O'Shea, M. & Adams, M. (1981). Pentapeptide (Proctolin: Arg-TrypLeu-Pro-Thr) associated with an identified neuron. Science 213, 567–569.CrossRefGoogle ScholarPubMed
Reichardt, W. & Poggio, T. (1976). Visual control of orientation behaviour in the fly, I: A quantitative analysis of neural interactions. Quarterly Review of Biophysics 9, 311–375.CrossRefGoogle Scholar
Reichardt, W., Poggio, T. & Hausen, K. (1983). Figure-ground discrimination by relative movement in the visual system of the fly, II: Towards the neural circuitry. Biological Cybernetics 46, 1–30.CrossRefGoogle Scholar
Ribi, W. (1983). Electron microscopy of Golgi-impregnated neurons. In Functional Neuroanatomy, ed. Strausfeld, N.J., pp. 1–18. Berlin, Heidelberg, New York: Springer Verlag.Google Scholar
Rossel, S. (1989). Binocular spatial localization in the preying mantis. Journal of Experimental Biology 120, 265–281.CrossRefGoogle Scholar
Smola, U. & Meffert, P. (1979). The spectral sensitivity of the visual cells R7 and R8 in the eye of the blowfly (Calliphora erythrocephala). Journal of Comparative Physiology 133, 41–52.CrossRefGoogle Scholar
Spurr, A. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructural Research 26, 31–43.CrossRefGoogle ScholarPubMed
Srinivasan, M.V. (1985). Shouldn't directional movement detection necessarily be “colour-blind?” Vision Research 25, 31–43CrossRefGoogle ScholarPubMed
Srinivasan, M.V. & Bernard, G.D. (1977). The pursuit of the housefly and its interaction with the optomotor response. Journal of Comparative Physiology A 115, 100–117CrossRefGoogle Scholar
Srinivasan, M.V. & Guy, R.G. (1990). Spectral properties of movement perception in the dronefly (Eristalis). Journal of Comparative Physiology A 166, 287–295CrossRefGoogle Scholar
Srinivasan, M.V., Lehrer, M., Zhang, S.W. & Horridge, G.A. (1989). How honeybees measure their distance from objects of unknown size. Journal of Comparative Physiology A 165, 605–613CrossRefGoogle Scholar
Strausfeld, N.J. (1970). Golgi studies on insects, II: The optic lobes of Diptera. Philosophical Transactions of the Royal Society B (London) 258, 135–223Google Scholar
Strausfeld, N.J. (1971). The organisation of the insect visual system (light microscopy), I: Projections and arrangements of neurones in the lamina ganglionaris of Diptera. Zeitschrift für Zellforschung 121, 377–441CrossRefGoogle Scholar
Strausfeld, N.J. (1976). Atlas of an Insect Brain. Heidelberg, New York, Berlin: Springer Verlag.CrossRefGoogle Scholar
Strausfeld, N.J. (1980). Male and female visual neurons in dipterous insects. Nature 283, 381–383CrossRefGoogle Scholar
Strausfeld, N.J. (1984). Functional neuronanatomy of the blowfly's visual system. In Photoreception and Vision in Invertebrates, ed. Ali, M.A. pp. 483–522New York: Plenum.CrossRefGoogle Scholar
Strausfeld, N.J. (1991) Structured organization of male-specific visual neurons in calliphorid optic lobes. Journal of Comparative Neurology 168 (in press).Google Scholar
Strausfeld, N.J. & Arakaki, C. (1990). In flies, motor neurons supplying indirect (power) and direct (steering) flight muscles occupy discrete neuropils supplied by characteristic motion-sensitive descending neurons. Society for Neuroscience Abstracts 16, 1225.Google Scholar
Strausfeld, N.J. & Bacon, J.P. (1982). Multimodal convergence in the central nervous system of insects. In Multimodal Convergence in Sensory Systems, ed. Horn, E., pp. 47–76Stuttgart: Gustav Fischer Verlag.Google Scholar
Strausfeld, N.J. & Bassemir, U.K. (1983). Cobalt-coupled neurons of a giant fibre system in Diptera. Journal of Neurocytology 12, 971–991CrossRefGoogle ScholarPubMed
Strausfeld, N.J. & Bassemir, U.K. (1985a). Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg neuropil in Calliphora erythrocephala. Cell and Tissue Research 240, 617–640CrossRefGoogle Scholar
Strausfeld, N.J. & Bassemir, U.K. (1985b). The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica. Cell and Tissue Research 242, 531–550CrossRefGoogle Scholar
Strausfeld, N.J. & Campos-Ortega, J.A. (1977). Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195, 894–897CrossRefGoogle ScholarPubMed
Strausfeld, N.J. & Gronenberg, W. (1990). Descending neurons supplying the neck and flight motor of Diptera: organization and neuroanatomical relationships with visual pathways. Journal of Comparative Neurology 302, 954–972CrossRefGoogle ScholarPubMed
Strausfeld, N.J. & Hausen, K. (1977). The resolution of neuronal assemblies after cobalt-injection into neuropil. Proceedings of the Royal Society B (London) 199, 463–476Google Scholar
Strausfeld, N.J. & NÄSsel, D.R. (1980). Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and insects. In Handbook of Sensory Physiology, Vii/6B, ed. Autrum, H., pp. 1–132Heidelberg, New York, Berlin: Springer Verlag.Google Scholar
Strausfeld, N.J. & Obermayer, M. (1975). Resolution of intraneuronal and transsynaptic migration of cobalt in the insect visual and nervous systems. Journal of Comparative Physiology 110, 1–12CrossRefGoogle Scholar
Strausfeld, N.J. & Seyan, H.S. (1987). Identification of complex neuronal arrangements in the visual system of Calliphora erythrocephala using triple fluorescence staining. Cell and Tissue Research 247, 5–10CrossRefGoogle Scholar
Strausfeld, N.J. & Wunderer, H. (1985). Optic lobe projections of marginal ommatidia in Calliphora erythrocephala specialized for detecting polarized light. Cell and Tissue Research 242, 163–178CrossRefGoogle Scholar
Strausfeld, N.J., Seyan, H.S. & Milde, J.J. (1987). The neck motor system of the fly (Calliphora erythrocephala), I: Muscles and motor neurons. Journal of Comparative Physiology A 160, 205–224CrossRefGoogle Scholar
Venable, J.H. & Coggeshall, R. (1965).A simplified lead citrate stain for use in electronmicroscopy. Journal of Cell Biology 25, 407–408CrossRefGoogle Scholar
Viallanes, H. (1897a). Études histologiques et organologiques sur lescentres nerveux et les organes des sens des animaux articulés. Quatrième mémoire. Le cerveau de la guèpe (Vespa crabro et V. vulgaris). Annals Scientifique Naturelles (Zoologie) (7) 2, 5–100Google Scholar
Viallanes, H. (1897b). Études histologiques et organologiques sur les centres nerveux et les organes des sens des animaux articulés. Quinquième mémoire. Le cerveau du Criquet (Oedopda coerulesens et Calopterus italicus). Annals Scientifique Naturelles (Zoologie) (7)4, 1–98Google Scholar
Von Frisch, K. (1914). Der Farbensinn und Formensinn der Biene. Zoologisches Jahrbuch (allgemeine Zoologie) 35, 1–182Google Scholar
Wagner, H. (1986a). Flight performance and visual control of flight of the free-flying housefly (Musca domestrica L), I: Pursuit of targets. Philosophical Transactions of the Royal Society B (London) 312, 533–579Google Scholar
Wagner, H. (1986b). Flight performance and visual control of flight of the free-flying housefly (Musca domestica L) I: Interactions between angular movement induced by wide- and small-field stimuli. Philosophical Transactions of the Royal Society B (London) 312, 581–595.Google Scholar