Skip to main content

Functional Neuroanatomy of the Blowfly’s Visual System

  • Chapter

Part of the book series: NATO ASI Series ((NSSA,volume 74))

Abstract

Outputs from the optic lobes arise mainly in the lobula (Lo) and lobula plate (LP), two neuropils each with distinct architectures. Columnar neurons, comprising the relatively large and multilayered Lo, receive the majority of axons originating in the peripheral medulla (Me). In contrast, the LP is a thin tectum of neuropil characterized by large field tangential cells thought to be involved in visual stabilization of flight. In common with other areas, relays from the retina into the LP are retinotopically organized. Neuroanatomical studies show that pathways destined for the Lo and LP segregate peripherally at the level of synapses between receptors and interneurons. The final input to the LP is carried by four identical neurons (the T4-pair and T5-pair), each quartet representing a point in the visual field which overlaps six surrounding points. The terminals of the quartet define two functional layers in the LP neuropil (horizontality and verticality). T-cell endings are presynaptic to horizontal (HS) and vertical (VS) motion sensitive neurons. Their synaptology suggests that computation of direction (as opposed to motion) is performed in the lobula plate. HS and VS cells input to separate channels leading out of the brain (sets of descending neurons, the DNHS and DNVS). The DNHS receive additional inputs from the antennae whereas the DNVS receive additional inputs from the ocelli. It is proposed that the DNVS set carries information about pitch, yaw and roll whereas the DNHS set carries information about angular acceleration and apparent speed of the visual surround.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   109.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Arnett, D.W. (1972) Spatial and temporal integration properties of units in the first optic ganglion of dipterans. J. Neurophysiol. 35: 429–444.

    Google Scholar 

  • Barlow, H.B. & Levick, W.R. (1965) The mechanism of directionally sensitive units in rabbit’s retina. J. Physiol. 178: 477–504.

    Google Scholar 

  • Beersma, D.G.M., Stavenga, D.G. & Kuiper, J.W. (1975) Organization of visual axes in the compound eye of the fly Musca domestica L. and behavioural consequences. J. Comp. Physiol. 102: 305–320.

    Article  Google Scholar 

  • Boschek, C.B. (1971) On the fine structure of the peripheral retina and lamina ganglionaris of the fly Musca domestica. Z. Zellforsch. 118: 369–409.

    Article  Google Scholar 

  • Braitenberg, V. (1967) Patterns of projections in the visual system of the fly. I. Retina-lamina projections. Exp. Brain Res. 3: 271–298.

    Article  Google Scholar 

  • Braitenberg, V. (1972) Periodic structures and structural gradients in the visual ganglia of the fly. In: Information Processing in the Visual System of Arthropods. Ed. R. Wehner. Berlin, Heidelberg, New York, Springer, p. 1–15.

    Google Scholar 

  • Braitenberg, V. & Debbage, P. (1974) A regular net of reciprocal synapses in the visual system of the fly Musca domestica. J. Comp. Physiol. 90: 25–31.

    Article  Google Scholar 

  • Buchner, E. (1976) Elementary movement detectors in an insect visual system. Biol. Cybern. 24: 85–101.

    Article  Google Scholar 

  • Buchner, E. & Buchner, S. (1983) Neuroanatomical mapping of visually induced nervous activity in insects by 3H-deoxyglucose. (This volume)

    Google Scholar 

  • Buchner, R., Buchner, S. & Hengstenberg, R. (1979) 2-deoxy-D-glucose maps movement-specific nervous activity in the second visual ganglion of Deosophila. Science 205: 687–688.

    Article  Google Scholar 

  • Cajal, S.R. & Sanchez, D. (1975) Contribution al conocimiento de los céntros nerviosos de los inséctos. Parte I, retina y centros opticos. Trab. Lab. Invest. Biol. Univ. Madrid 13: 1–168.

    Google Scholar 

  • Campos-Ortega, J.A. (1982) Development of the nervous system. In: Handbook of Drosophila Development. Ed. R. Ransom. Amsterdan, New York, Oxford, Elsevier Biomedical.

    Google Scholar 

  • Campos-Ortega, J.A. & Strausfeld, N.J. ( 1972 a) 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 System of Arthropods. Ed. R. Wehner. Berlin, Heidelberg, New York, Springer.

    Google Scholar 

  • Campos-Ortega J.A. & Strausfeld, N.J. ( 1972 b) The columnar organization of the second synaptic region of the visual system of Musca domestica L. I. Receptor terminals in the medulla. Z. Zellforsch. 124: 561–585.

    Article  Google 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 Res. 59: 119–136.

    Article  Google Scholar 

  • Dvorak, D.R., Bishop, L.G. & Eckert, H.E. (1975) On the identification of movement detectors in the fly optic lobe. J. Comp. Physiol. 100: 5–23.

    Article  Google Scholar 

  • Eckert, H. (1981) The horizontal cells in the lobula plate of the blowfly, Phaenicia sericata. J. Comp. Physiol. 143: 511–526.

    Article  Google Scholar 

  • Eckert, H. (1982) The vertical-horizontal neurone (VH) in the lobula plate of the blowfly, Phaenicia. J. Comp. Physiol. 149: 195–205.

    Article  Google Scholar 

  • Eckert, H. & Bishop, L.G. (1978) Anatomical and physiological properties of the vertical cells in the third optic ganglion of Phaenicia sericata ( Diptera, Calliphoridae). J. Comp. Physiol. 126: 57–86.

    Article  Google Scholar 

  • Fischbach, K.F. (1983) Neural cell types surviving congential sensory deprivation in the optic lobes of Drosophila melanogaster. Dev. Biol. 95: 1–18.

    Article  Google Scholar 

  • Franceschini, N. (1975) Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In: Photoreceptor Optics. Ed. A.W. Snyder & R. Menzel. Berlin, Heidelberg, New York, Springer, p. 97–125.

    Google Scholar 

  • Franceschini, N., Hardie, R., Ribi, R. & Kirschfeld, K. (1981) Sexual dimorphism in a photoreceptor. Nature (Lond.) 291: 241–244.

    Article  Google Scholar 

  • Gewecke, M. (1974) The antennae of insects as air current sense organs and their relationships to the control of flight. In: Experimental Analysis of Insect Behaviour. Ed. L. Barton-Browne. Berlin, Heidelberg, New York, Springer, p. 100–113.

    Chapter  Google Scholar 

  • Hausen, K. (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh. Dtsch. Zool. Ges. 1981: 47–70

    Google Scholar 

  • Hausen, K. ( 1982 a) Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol. Cybern. 45: 143–156.

    Article  Google Scholar 

  • Hausen, K. ( 1982 b) Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: receptive field organization and response characteristics. Biol. Cybern. 46: 67–79.

    Article  Google Scholar 

  • Hausen, K. & Strausfeld, N.J. (1980) Sexually dimorphic interneuron arrangements in the fly visual system. Proc. R. Soc. Lond. 208B: 57–71.

    Article  Google Scholar 

  • Hengstenberg, R. (1977) Spike responses of “non-spiking” visual interneurones. Nature (Lond.) 270: 338–340.

    Article  Google Scholar 

  • Hengstenberg, R. (1982) Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J. Comp. Physiol. 149: 179–193.

    Article  Google Scholar 

  • Hengstenberg, R., Bülthoff, H. & Hengstenberg, B. (1983) Three-dimensional reconstruction and stereoscopic display of neurons in the fly visual system. In: Functional Neuroanatomy. Ed. N.J. Strausfeld. Springers series in Experimental Entomology. Heidelberg, Berlin, New York, Springer. (In press)

    Google Scholar 

  • Hengstenberg, R., Hausen, K. & Hengstenberg, B. (1982) The number and structure of giant vertical cells (VS) in the lobula plate of the blowfly Calliphora erythrocephala. J. Comp. Physiol. 149: 163–178.

    Article  Google Scholar 

  • Hubel, D.H. & Wiesel, T.N. (1974) Sequence, regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158: 267–294.

    Article  Google Scholar 

  • 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. 136: 291–306.

    Article  Google Scholar 

  • Kirschfeld, K. (1967) Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Exp. Brain Res. 2: 248–270.

    Google Scholar 

  • Laughlin, S.B. (1973) Neural integration in the first optic neuropil of dragonflies. I. Signal amplification in dark-adapted second-order neurons. J. Comp. Physiol. 84: 335–355.

    Article  Google Scholar 

  • Laughlin, S.B. (1974) Neural integration in the first optic neuropile of dragonflies. III. The transfer of angular information. J. Comp. Physiol. 99: 377–396.

    Google Scholar 

  • Laughlin, S.B. (1975) Receptor and interneurone light adaptation in the dragonfly visual system. Z. Naturf. 30c: 306–308.

    Google Scholar 

  • Laughlin, S.B. (1976) Neural integration in the first optic neuropile of dragonflies. IV. Interneurone spectral sensitivity and contrast coding. J. Comp. Physiol. 122: 199–211.

    Article  Google Scholar 

  • Laughlin, S.B. (1981) Neural principles in the visual system. In: Handbook of Sensory Physiology. Vol. VII/6B. Ed. H. Autrum. Berlin, Heidelberg, New York, Springer.

    Google Scholar 

  • Laughlin, S.B. & Hardie, R.C. (1978) Common strategies for light adaptation in the peripheral visual system of fly and dragonfly. J. Comp. Physiol. 128: 319–340.

    Article  Google Scholar 

  • Mclntyre, P. & Snyder, A.W. (1978) Light propagation in twisted anisotropic media: application to photoreceptors. J. Opt. Soc. Am. 68: 149–157.

    Article  Google Scholar 

  • Meinertzhagen, I.A. (1973) Development of the compound eye and optic lobes of insects. In: Developmental Neurobiology of Arthropods. Ed. D. Young. Cambridge, London, New York, Cambridge University Press, p. 51–104.

    Google Scholar 

  • Meinertzhagen, I.A. (1976) The organization of perpendicular fibre pathways in the insect optic lobe. Phil. Trans. R. Soc. Lond. 274B: 555–596.

    Google Scholar 

  • Melamed, J. & Trujillo-Cenoz, O. (1968) The fine structure of the central cells in the ommatidia of dipterans. J. Ultrastruct. Res. 21: 313–334.

    Article  Google Scholar 

  • Pierantoni, R. (1976) A look into the cock-pit of the fly: the architecture of the lobular plate. Cell Tissue Res. 171: 101–122.

    Article  Google Scholar 

  • Ready, D.F., Hanson, T.E. & Benzer, S. (1976) Development of the Drosophila retina. A neurocrystalline lattice. Dev. Biol. 53: 217–240.

    Article  Google Scholar 

  • Ribi, W.A. (1975) The neurons of the first optic ganglion of the bee Apis mellifera. Adv. Anat. Embryol. Cell Biol. 50: 1–43.

    Google Scholar 

  • Rowell, C.H.F., O’Shea, M. & Williams, J.L.D. (1977) The neuronal basis of a sensory analyser, the acridid moment detector system. IV. The preference for small field stimuli. J. Exp. Biol. 68: 157–185.

    Google Scholar 

  • Scholes, J. (1969) The electrical responses of the retina receptors and the lamina in the visual system of the fly Musca. Kybernetik 6: 149–162.

    Article  Google Scholar 

  • Shaw,S.R. (1975) Retinal resistance barriers and electrical lateral inhibition. Nature (Lond.) 255: 480–482.

    Article  Google Scholar 

  • Shaw,S.R. (1981) Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially diptera. In: Neurons without Impulses. Ed. A. Roberts & B.M.H. Bush. Cambridge, London, New York, Cambridge University Press.

    Google Scholar 

  • Srinivasan, M.V. & Bernard, G.D. (1975) The effect of motion of visual acuity of the compound eye: a theoretical analysis. Vision Res. 15: 515–525.

    Google Scholar 

  • Stavenga, D.G. (1979) Pseudopupils of compound eyes. In: Handbook of Sensory Physiology. Vol. VII/6A. Ed. H. Autrum. Heidelberg, Berlin, New York, Springer, p. 357–439.

    Google Scholar 

  • Strausfeld, N.J. (1970) Golgi studies on insects. Part II. The optic lobes of diptera. Phil. Trans. R. Soc. Lond. 258B: 175–223.

    Google Scholar 

  • Strausfeld, N.J. (1971) The organization of the insect visual system (light microscopy). II. The projection of fibres across the first optic chiasma. Z. Zellforsch. 121: 442–454.

    Article  Google Scholar 

  • Strausfeld, N.J. ( 1976 a) Mosaic organizations, layers, and visual pathways in the insect brain. In: Neural Principles in Vision. Ed. F. Zettler & R. Weiler. Berlin, Heidelberg, New York, Springer.

    Google Scholar 

  • Strausfeld, N.J. ( 1976 b) Atlas of an Insect Brain. Berlin, Heidelberg, New York, Springer.

    Book  Google Scholar 

  • Strausfeld, N.J. (1979) The representation of a receptor map within retinotopic neuropil of the fly. Verh. Dtsch. Zool. Ges. 1979: 167–177.

    Google Scholar 

  • Strausfeld, N.J. (1980) Male and female neurons in dipterous insects. Nature (Lond.) 233: 381–383.

    Article  Google Scholar 

  • Strausfeld, N.J. & Bacon, J.P. (1983) Multimodal convergence in the central nervous system of insects. In: Multimodal Convergence in Sensory Systems. Fortschr. Zool. 28. Ed. E. Horn. Stuttgart, New York, Gustav Fischer.

    Google Scholar 

  • Strausfeld, N.J. & Bassemir, U.K. (1983) Cobalt-coupled neurons of a giant fiber system in Diptera. J. Neurocytol. (In press)

    Google Scholar 

  • Strausfeld, N.J., Bassemir, U.K., Singh, R.N. & Bacon, J.P. (1983) Organizational principles of outputs from dipteran brains. J. Insect Physiol. (In press)

    Google Scholar 

  • Strausfeld, N.J. & Blest, A.D. (1970) Golgi studies on insects. Part I. The optic lobes of Lepidoptera. Phil. Trans. R. Soc. Lond. 258B: 81–134.

    Google Scholar 

  • Strausfeld, N.J. & Braitenberg, V. (1970) The compound eye of the fly (Musca domestica): connections between the cartridges of the lamina ganglionaris. Z. vergl. Physiol. 70: 95–104.

    Article  Google Scholar 

  • Strausfeld, N.J. & Campos-Ortega, J.A. (1977) Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195: 894–897.

    Article  Google Scholar 

  • Strausfeld, N.J. & Hausen, K. (1977) The resolution of neuronal assemblies after cobalt injection into neuropil. Proc. R. Soc. Lond. 199B: 563–476.

    Google Scholar 

  • Strausfeld, N.J. & Nässel, D.R. (1981) Neuroarchitecture of brain regions that subserve the compound eyes of crustacea and insects. In: Handbook of Sensory Physiology. Vol. VII/6B. Ed. H. Autrum. Berlin, Heidelberg, New York, Springer.

    Google Scholar 

  • Taylor, C.P. (1981) Contribution of compound eyes and ocelli to steering of locusts in flight. 1. Behavioural analysis. J. Exp. Biol. 93: 1–18.

    Google Scholar 

  • Torre, V. & Poggio, T. (1978) A synaptic mechanism possibly underlying directional selectivity to motion. Proc. R. Soc. Lond. 202B: 409–416.

    Article  Google Scholar 

  • Trujillo-Cenoz, O. (1966) Some aspects of the structural organization of the intermediate retina of dipterans. J. Ultrastruct. Res. 13: 1–33.

    Article  Google Scholar 

  • Trujillo-Cenoz, O. & Melamed, J. (1966) Electron microscopical observations on the peripheral and intermediate retina of dipterans. In: The Functional Organization of the Compound Eye. Ed. C.G. Bernhard. London, Pergamon.

    Google Scholar 

  • Vigier, P. ( 1907 a) Méchanisme de la synthèse des impressions lumineuses recueillies par les yeux composés des Diptères. C.R. Acad. Sci. ( Paris ) 63: 122–124.

    Google Scholar 

  • Vigier, P. ( 1907 b) Sur les terminations photoréceptrices dans les yeux composés des Muscides. C.R. Acad. Sci. ( Paris ) 63: 532–536.

    Google Scholar 

  • Vigier, P. ( 1907 c) Sur la réception de l’excitant lumineux dans les yeux composés des insectes, en particulier chez les Muscides. C.R. Acad. Sci. ( Paris ) 63: 633–636.

    Google Scholar 

  • Vigier, P. (1908) Sur l’existence réelle et le rôle des appendices piriform des neurones. La neurone périoptique des Diptères. C.R. Soc. Biol. ( Paris ) 64: 959–961.

    Google Scholar 

  • Wilson, M. (1978) Functional organization of locust ocelli. J. Comp. Physiol. 124: 297–316.

    Article  Google Scholar 

  • Wunderer, H. & Smola, U. ( 1982 b) Fine structure of ommatidia at the dorsal eye margin of Calliphora erythrocephala Meigen (Diptera: Calliphoridae): an eye region specialized for the detection of polarized light. Int. J. Insect Morphol. Embryol. 11: 25–38.

    Article  Google Scholar 

  • Zettler, F. & Järvilheto, M. (1971) Decrement-free conduction of graded potentials along the axon of a monopolar neuron. Z. vergl. Physiol. 75: 402–421.

    Article  Google Scholar 

  • Zettler, F. & Järvilheto, M. (1972) Lateral inhibition in an insect eye. Z. vergl. Physiol. 76: 233–244.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1984 Plenum Press, New York

About this chapter

Cite this chapter

Strausfeld, N.J. (1984). Functional Neuroanatomy of the Blowfly’s Visual System. In: Ali, M.A. (eds) Photoreception and Vision in Invertebrates. NATO ASI Series, vol 74. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2743-1_14

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-2743-1_14

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-9699-7

  • Online ISBN: 978-1-4613-2743-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics