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.
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References
Arnett, D.W. (1972) Spatial and temporal integration properties of units in the first optic ganglion of dipterans. J. Neurophysiol. 35: 429–444.
Barlow, H.B. & Levick, W.R. (1965) The mechanism of directionally sensitive units in rabbit’s retina. J. Physiol. 178: 477–504.
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.
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.
Braitenberg, V. (1967) Patterns of projections in the visual system of the fly. I. Retina-lamina projections. Exp. Brain Res. 3: 271–298.
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.
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.
Buchner, E. (1976) Elementary movement detectors in an insect visual system. Biol. Cybern. 24: 85–101.
Buchner, E. & Buchner, S. (1983) Neuroanatomical mapping of visually induced nervous activity in insects by 3H-deoxyglucose. (This volume)
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.
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.
Campos-Ortega, J.A. (1982) Development of the nervous system. In: Handbook of Drosophila Development. Ed. R. Ransom. Amsterdan, New York, Oxford, Elsevier Biomedical.
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.
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.
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.
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.
Eckert, H. (1981) The horizontal cells in the lobula plate of the blowfly, Phaenicia sericata. J. Comp. Physiol. 143: 511–526.
Eckert, H. (1982) The vertical-horizontal neurone (VH) in the lobula plate of the blowfly, Phaenicia. J. Comp. Physiol. 149: 195–205.
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.
Fischbach, K.F. (1983) Neural cell types surviving congential sensory deprivation in the optic lobes of Drosophila melanogaster. Dev. Biol. 95: 1–18.
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.
Franceschini, N., Hardie, R., Ribi, R. & Kirschfeld, K. (1981) Sexual dimorphism in a photoreceptor. Nature (Lond.) 291: 241–244.
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.
Hausen, K. (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh. Dtsch. Zool. Ges. 1981: 47–70
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.
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.
Hausen, K. & Strausfeld, N.J. (1980) Sexually dimorphic interneuron arrangements in the fly visual system. Proc. R. Soc. Lond. 208B: 57–71.
Hengstenberg, R. (1977) Spike responses of “non-spiking” visual interneurones. Nature (Lond.) 270: 338–340.
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.
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)
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.
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.
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.
Kirschfeld, K. (1967) Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Exp. Brain Res. 2: 248–270.
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.
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.
Laughlin, S.B. (1975) Receptor and interneurone light adaptation in the dragonfly visual system. Z. Naturf. 30c: 306–308.
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.
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.
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.
Mclntyre, P. & Snyder, A.W. (1978) Light propagation in twisted anisotropic media: application to photoreceptors. J. Opt. Soc. Am. 68: 149–157.
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.
Meinertzhagen, I.A. (1976) The organization of perpendicular fibre pathways in the insect optic lobe. Phil. Trans. R. Soc. Lond. 274B: 555–596.
Melamed, J. & Trujillo-Cenoz, O. (1968) The fine structure of the central cells in the ommatidia of dipterans. J. Ultrastruct. Res. 21: 313–334.
Pierantoni, R. (1976) A look into the cock-pit of the fly: the architecture of the lobular plate. Cell Tissue Res. 171: 101–122.
Ready, D.F., Hanson, T.E. & Benzer, S. (1976) Development of the Drosophila retina. A neurocrystalline lattice. Dev. Biol. 53: 217–240.
Ribi, W.A. (1975) The neurons of the first optic ganglion of the bee Apis mellifera. Adv. Anat. Embryol. Cell Biol. 50: 1–43.
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.
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.
Shaw,S.R. (1975) Retinal resistance barriers and electrical lateral inhibition. Nature (Lond.) 255: 480–482.
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.
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.
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.
Strausfeld, N.J. (1970) Golgi studies on insects. Part II. The optic lobes of diptera. Phil. Trans. R. Soc. Lond. 258B: 175–223.
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.
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.
Strausfeld, N.J. ( 1976 b) Atlas of an Insect Brain. Berlin, Heidelberg, New York, Springer.
Strausfeld, N.J. (1979) The representation of a receptor map within retinotopic neuropil of the fly. Verh. Dtsch. Zool. Ges. 1979: 167–177.
Strausfeld, N.J. (1980) Male and female neurons in dipterous insects. Nature (Lond.) 233: 381–383.
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.
Strausfeld, N.J. & Bassemir, U.K. (1983) Cobalt-coupled neurons of a giant fiber system in Diptera. J. Neurocytol. (In press)
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)
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.
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.
Strausfeld, N.J. & Campos-Ortega, J.A. (1977) Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195: 894–897.
Strausfeld, N.J. & Hausen, K. (1977) The resolution of neuronal assemblies after cobalt injection into neuropil. Proc. R. Soc. Lond. 199B: 563–476.
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.
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.
Torre, V. & Poggio, T. (1978) A synaptic mechanism possibly underlying directional selectivity to motion. Proc. R. Soc. Lond. 202B: 409–416.
Trujillo-Cenoz, O. (1966) Some aspects of the structural organization of the intermediate retina of dipterans. J. Ultrastruct. Res. 13: 1–33.
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.
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.
Vigier, P. ( 1907 b) Sur les terminations photoréceptrices dans les yeux composés des Muscides. C.R. Acad. Sci. ( Paris ) 63: 532–536.
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.
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.
Wilson, M. (1978) Functional organization of locust ocelli. J. Comp. Physiol. 124: 297–316.
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.
Zettler, F. & Järvilheto, M. (1971) Decrement-free conduction of graded potentials along the axon of a monopolar neuron. Z. vergl. Physiol. 75: 402–421.
Zettler, F. & Järvilheto, M. (1972) Lateral inhibition in an insect eye. Z. vergl. Physiol. 76: 233–244.
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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
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