Journal of comparative physiology

, Volume 124, Issue 4, pp 297–316

The functional organisation of locust ocelli

  • Martin Wilson
Article

Summary

This paper examines the optical and physiological organisation of locust ocelli with a view to understanding their function. The approach taken in this work has largely been to correlate quantitative measurements of the spectral, angular and absolute sensitivities of large second order neurons with radiometric data from the natural environment. The resulting estimates of the natural performance of these neurons form the basis for a hypothesis of their functional significance.
  1. 1.

    In both median and lateral ocelli of adult locusts the image plane lies well behind the retina regardless of pupil diameter. It is pointed out that underfocussing confers positive advantages and should be seen as an integral part of ocellar design.

     
  2. 2.

    The ocellar nerves contain axons that carry graded hyperpolarisations and axons that carry trains of action potentials. Graded potentials are identified with the large (L) neurons. The spiking axons, of which some are light-inhibited and some are light-excited, are thought to be the small (S) neurons.

     
  3. 3.

    Constriction of the radial pupil during light adaptation causes little diminution of the total field of view of an ocellus. The horizontal extent of the visual fields of L neurons in lateral ocelli, measured electrophysiologically is about 140°, effectively that of the whole retina. These wide fields are consistent with the underfocussed dioptrics and the reported extensive branching of these cells in the subretinal neuropile.

     
  4. 4.

    Dark adaptation of L neurons following normal preparative procedures takes several hours and increases sensitivity by over 3 log units. Complete dark adaptation is associated with large (up to 10 mV average amplitude) hyperpolarising bumps clearly distinguishable from noise and presumed to result from single photon captures.

     
  5. 5.

    Using an index of sensitivity that relates to monochromatic stimulation of an eye with an axial point source it is estimated that L neurons are 5 × more sensitive than compound eye lamina neurons but to an extended source they would be 5000 × more sensitive.

     
  6. 6.

    Of 18 L neurons whose spectral sensitivity was examined, all had maximum sensitivity close to 370 nm. A secondary peak at 500 nm varied in height from cell to cell between 48% and 0.3% of the UV peak. One cell was found in the median ocellus that showed stronger inhibition from green than UV stimuli. It is concluded that color coding by the ocellus is possible.

     
  7. 7.

    It is suggested that the disposition of locust ocelli, the spectral sensitivity and the temporal and spatial filtering characteristics of their L neurons suit these cells well to the task of detecting instability in flight. This idea is discussed in relation to the anatomy and physiology of ocellar pathways.

     

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References

  1. Autrum, H., Metschl, N.: Beziehungen zwischen Lichtreiz und Erregung im Ocellusnerven vonCalliphora erythrocephala. Z. Naturforsch.16b, 384–388 (1961)Google Scholar
  2. Autrum, H., Zettler, F., Järvilehto, M.: Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowflyCalliphora. Z. vergl. Physiol.70, 414–424 (1970)Google Scholar
  3. Brousse-Gaury, P.: Description d'arcs réflexes neuroendocriniens partant des ocelles chez quelques Orthoptères. Bull. biol. France Belg.105, 83–93 (1971)Google Scholar
  4. Brown, K.T., Flaming, D.G.: Instrumentation and technique for bevelling fine micropipette electrodes. Brain Res.86, 172–180 (1975)Google Scholar
  5. Buddenbrock, W. von: Grundriss der vergleichenden Physiologie. Berlin: Borntraeger 1937Google Scholar
  6. Burkhardt, D., Streck, P.: Das Sehfeld einzelner Sehzellen: eine Richtigstellung. Z. vergl. Physiol.51, 151–152 (1965)Google Scholar
  7. Burtt, E.T., Catton, W.T.: Visual perception of movement in the locust. J. Physiol. (Lond.)125, 566–580 (1954)Google Scholar
  8. Cajal, S.R.: Observaciones sobre la estructura de los ocelos y vias nerviosas ocelares de algunos insectos. Trab. Lab. Invest. Biol. Univ. Madrid16, 109–139 (1918)Google Scholar
  9. Callec, J.J.: Etude de la transmission synaptique dans le système nerveux central d'un insecte (Periplanteta americana). Doctoral thesis, University of Rennes 1972Google Scholar
  10. Chappell, R.L., DeVoe, R.D.: Action spectra and chromatic mechanisms of cells in the median ocelli of dragonflies. J. gen. Physiol.65, 399–419 (1975)Google Scholar
  11. Chappell, R.L., Dowling, J.E.: Neural organization of the median ocellus of the dragonfly. I. Intracellular electrical activity. J. gen. Physiol.60, 121–147 (1972)Google Scholar
  12. Clark, D.P.: Flights after sunset by the Australian plague locust,Chorioicetes terminifera (Walk.), and their significance in dispersal and migration. Aust. J. Zool.19, 159–176 (1971)Google Scholar
  13. Cornwell, P.B.: The functions of the ocelli ofCalliphora (Diptera) andLocusta (Orthoptera). J. exp. Biol.32, 217–237 (1955)Google Scholar
  14. Dartnall, H.J.A.: Photosensitivity. In: Handb. sens. physiol., Vol. VII/I (ed. H.J.A. Dartnall). Berlin-Heidelberg-New York: Springer 1972Google Scholar
  15. Demoll, R., Scheuring, L.: Die Bedeutung der Ocellen der Insecten. Zool. Jb. (Abt. Zool. Physiol.)31, 519–628 (1912)Google Scholar
  16. Dickens, J.C., Eaton, J.L.: Fine structure of ocelli in sphinx moths. Tissue and Cell6, 463–470 (1974)Google Scholar
  17. Dow, M.A., Eaton, J.L.: Fine structure of the ocellus of the cabbage looper moth (Trichoplusia ni). Cell Tiss. Res.171, 523–533 (1976)Google Scholar
  18. Dowling, J.E., Chappell, R.L.: Neural organization of the median ocellus of the dragonfly. II. Synaptic structure. J. gen. Physiol.60, 148–165 (1972)Google Scholar
  19. Eaton, J.L.: Electroretinogram components of the ocellus of the adult cabbage looper mothTrichoplusia ni. J. Insect Physiol.21, 1511–1516 (1975)Google Scholar
  20. Eaton, J.L.: Spectral sensitivity of the ocelli of the adult cabbage looper mothTrichoplusia ni. J. comp. Physiol.109, 17–24 (1976)Google Scholar
  21. Erber, J., Sandeman, D.C.: The detection of real and apparent motion by the crabLeptograpsus variegatus. II. Electrophysiology. J. comp. Physiol.112, 189–197 (1976)Google Scholar
  22. Farrow, R.A.: The African migratory locust in its main outbreak area of the middle Niger: Quantitative studies of solitary populations in relation to environmental factors. Locusta11, 1–198 (1975a)Google Scholar
  23. Farrow, R.A.: Offshore migration and the collapse of outbreaks of the Australian plague locust (Chortoicetes terminifera Walk.) in South East Australia. Aust. J. Zool.23, 569–595 (1976b)Google Scholar
  24. Goldsmith, T.H., Ruck, P.R.: The spectral sensitivities of the dorsal ocelli of cockroaches and honeybees. J. gen. Physiol.41, 1171–1185 (1958)Google Scholar
  25. Goodman, C.S.: Anatomy of locust ocellar interneurons: constancy and variability. J. comp. Physiol.95, 185–201 (1974)Google Scholar
  26. Goodman, C.S.: Constancy and uniqueness in a large population of small interneurons. Science193, 502–504 (1976a)Google Scholar
  27. Goodman, C.S.: Anatomy of the ocellar interneurons of Acridid grasshoppers. I. The large interneurons. Cell Tiss. Res.175, 166–183 (1976b)Google Scholar
  28. Goodman, C.S., Williams, J.L.D.: Anatomy of locust ocellar interneurons. II. The small interneurons. Cell Tiss. Res.175, 184–203 (1976)Google Scholar
  29. Goodman, L.J.: The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locust,Schistocerca gregaria. J. exp. Biol.42, 382–407 (1965)Google Scholar
  30. Goodman, L.J.: The structure and function of the insect dorsal ocellus. Advanc. Insect. Physiol.7, 97–195 (1970)Google Scholar
  31. Goodman, L.J.: The neural organization and physiology of the insect dorsal ocellus. In: The compound eye and vision of insects (ed. G.A. Horridge). Oxford: Oxford University Press 1975Google Scholar
  32. Goodman, L.J., Patterson, J.A., Mobbs, P.G.: The projection of ocellar neurons within the brain of the locust,Schistocerca gregaria. Cell Tiss. Res.157, 467–492 (1975)Google Scholar
  33. Hapke, B.: Optical properties of the lunar surface. In: Physics and astronomy of the moon, 2 Ed. (ed. Z. Kopal), pp. 155–209. New York-London: Academic Press 1971Google Scholar
  34. Heinzeller, T.: Second-order ocellar neurons in the brain of the honey bee (Apis mellifera). Cell Tiss. Res.171, 91–99 (1976)Google Scholar
  35. Homann, H.: Zum Problem der Ocellenfunktion bei den Insekten. Z. vergl. Physiol.1, 541–578 (1924)Google Scholar
  36. Honegger, H.-W., Schürmann, F.W.: Cobalt sulfide staining of optic fibres in the brain of the cricket,Gryllus campestris. Cell Tiss. Res.159, 213–225 (1975)Google Scholar
  37. Hoyle, G.: Functioning of the insect ocellar nerve. J. exp. Biol.32, 397–407 (1955)Google Scholar
  38. Järvilehto, M., Zettler, F.: Localized intracellular potentials from pre- and postsynaplic components in the external plexiform layer of an insect retina. Z. vergl. Physiol.75, 422–440 (1971)Google Scholar
  39. Jander, R., Barry, C.K.: Die phototaktische Gegenkopplung von Stirnocellen und Facettenaugen in der Phototropotaxis der Heuschrecken und Grillen (Saltoptera:Locusta migratoria undGryllus bimaculatus). Z. vergl. Physiol.57, 432–458 (1968)Google Scholar
  40. Kalmus, H.: Correlations between flight and vision, and particularly between wings and ocelli in insects. Proc. roy. ent. Soc. Lond. A20, 84–96 (1945)Google Scholar
  41. Kenyon, F.C.: The brain of the bee. A preliminary contribution to the morphology of the nervous system of the Arthropoda. J. comp. Neurol.6, 133–210 (1896)Google Scholar
  42. Kolbe, H.G.: Einführung in die Kenntnis der Insekten. Berlin 1893Google Scholar
  43. Land, M.F.: Image formation by a concave reflector in the eye of the scallop,Pecten maximus. J. Physiol. (Lond.)179, 138–153 (1965)Google Scholar
  44. Land, M.F.: The physics and biology of animal reflectors. Progr. Biophys.24, 75–106 (1972)Google Scholar
  45. Langer, H.: Properties and functions of screening pigments in insect eyes. In: Photoreceptor optics (eds. A.W. Snyder, R. Menzel), pp. 429–458. Berlin-Heidelberg-New York: Springer 1975Google Scholar
  46. Laughlin, S.B.: Neural integration in the first optic neuropile of dragonflies. I. Signal amplification in dark-adapted second order neurons. J. comp. Physiol.84, 335–355 (1973)Google Scholar
  47. Laughlin, S.B.: Neural integration in the first optic neuropile of dragonflies. III. The transfer of angular information. J. comp. Physiol.92, 377–396 (1974)Google Scholar
  48. Laughlin, S.B.: The sensitivities of dragonfly photoreceptors and the voltage gain of transduction. J. comp. Physiol.111, 221–247 (1976a)Google Scholar
  49. Laughlin, S.B.: Neural integration in the first optic neuropile of dragonflies. IV. Interneuron spectral sensitivity and contrast coding. J. comp. Physiol.112, 199–211 (1976b)Google Scholar
  50. Link, E.: Über die Stirnaugen der hemimetabolen Insekten. Zool. Jb. Anat.27, 281–376 (1909)Google Scholar
  51. Menzel, R.: Spectral sensitivity of monopolar cells in the bee lamina. J. comp. Physiol.93, 337–346 (1974)Google Scholar
  52. Mimura, K., Tateda, H., Morita, H., Kuwabara, M.: Regulation of insect brain excitability by ocellus. Z. vergl. Physiol.62, 382–394 (1969)Google Scholar
  53. Mimura, K., Tateda, H., Morita, H., Kuwabara, M.: Convergence of antennal and ocellar inputs in the insect brain. Z. vergl. Physiol.68, 301–310 (1970)Google Scholar
  54. Mobbs, P.G.: Development of the locust ocellus. Nature (Lond.)264, 269–271 (1976)Google Scholar
  55. Naka, K.I., Rushton, W.A.H.: S-potentials from colour units in the retina of fish (Cyprinidae). J. Physiol. (Lond.)185, 536–555 (1966)Google Scholar
  56. Pan, K.C., Goodman, L.J.: Ocellar projections within the central nervous system of the worker honey beeApis mellifera. Cell Tiss. Res.176, 505–527 (1977)Google Scholar
  57. Parry, D.A.: The function of the insect ocellus. J. exp. Biol.24, 211–219 (1947)Google Scholar
  58. Patterson, J.A., Goodman, L.J.: Intracellular responses of receptor cells and second order cells in the ocelli of the desert locustSchistocerca gregaria. J. comp. Physiol.95, 237–250 (1974a)Google Scholar
  59. Patterson, J.A., Goodman, L.J.: Relationships between ocellar units in the ventral nerve cord and ocellar pathways in the brain ofSchistocerca gregaria. J. comp. Physiol.95, 251–262 (1974b)Google Scholar
  60. Pitman, R.M., Tweedle, C.D., Cohen, M.J.: The form of nerve cells: determination by cobalt impregnation. In: Intracellular staining in neurobiology (eds. S.B. Kater, C. Nicholson), pp. 83–98. Berlin-Heidelberg-New York: Springer 1973Google Scholar
  61. Ruck, P.: The electrical responses of dorsal ocelli in cockroaches and grasshoppers. J. Insect Physiol.1, 109–123 (1957)Google Scholar
  62. Ruck, P.: Dark adaptation of the ocellus inPeriplaneta americana: a study of the electrical response to illumination. J.Insect. Physiol.2, 189–198 (1958a)Google Scholar
  63. Ruck, P.: A comparison of the electrical responses of compound eyes and dorsal ocelli in four insect species. J. Insect Physiol.2, 261–274 (1958b)Google Scholar
  64. Ruck, P.: Electrophysiology of the insect dorsal ocellus. I. Origin of the components of the electroretinogram. J. gen. Physiol.44, 605–639 (1961)Google Scholar
  65. Ruck, P.: The components of the visual system of a dragonfly. J. gen. Physiol.49, 289–307 (1965)Google Scholar
  66. Ruck, P., Edwards, G.A.: The structure of the insect dorsal ocellus. J. Morph.115, 1–26 (1964)Google Scholar
  67. Shaw, S.R.: Organisation of the locust retina. Symp. Zool. Soc. Lond.23, 135–163 (1968)Google Scholar
  68. Sontag, C.: Spectral sensitivity studies on the visual system of the praying mantisTenodera sinensis. J. gen. Physiol.57, 93–112 (1971)Google Scholar
  69. Strausfeld, N.J.: Atlas of an insect brain. Berlin-Heidelberg-New York: Springer 1976Google Scholar
  70. Suzuki, H., Tateda, H., Kuwabara, M.: Activities of antennal and ocellar interneurons in the protocerebrum of the honey-bee. J. exp. Biol.64, 405–418 (1976)Google Scholar
  71. Thorson, J.: Small signal analysis of a visual reflex in the locust. I. Input parameters. Kybernetik3, 41–53 (1966)Google Scholar
  72. Toh, Y., Kuwabara, M.: Fine structure of the dorsal ocellus of the worker honeybee. J. Morph.143, 285–306 (1974)Google Scholar
  73. Toh, Y., Kuwabara, M.: Synaptic organization of the fleshfly ocellus. J. Neurocytol.4, 271–287 (1975)Google Scholar
  74. Toh, Y., Tominaga, Y., Kuwabara, M.: The fine structure of dorsal ocellus of the fleshfly. J. Electr. Microsc.20, 56–66 (1971)Google Scholar
  75. Usherwood, P.N.R., Grundfest, H.: Peripheral inhibition in skeletal muscle of insects. J. Neurophysiol.28, 497–518 (1965)Google Scholar
  76. Uvarov, B.: Grasshoppers and locusts, Vol. I. Cambridge: Cambridge University Press 1966Google Scholar
  77. Weber, G., Renner, M.: The ocellus of the cockroachPeriplaneta americana (Blattariae). Receptory area. Cell Tiss. Res.168, 209–222 (1976)Google Scholar
  78. Wellington, W.G.: Motor responses evoked by the dorsal ocelli ofSarcophaga aldrichi Parker and the orientation of the fly to plane polarised light. Nature (Lond.)172, 1177–1179 (1953)Google Scholar
  79. Wellington, W.G.: Bumblebee ocelli and navigation at dusk. Science183, 550–551 (1974)Google Scholar
  80. Werblin, F.S., Dowling, J.E.: Organization of the retina of the mudpuppy,Necturus maculosus. II. Intracellular recording. J. Neurophysiol.32, 339–355 (1969)Google Scholar
  81. Williams, J.L.D.: Anatomical studies of the insect central nervous system: A ground-plan of the midbrain and an introduction to the central complex in the locust,Schistocerca gregaria. J. Zool. (Lond.)176, 67–86 (1975)Google Scholar
  82. Wilson, D.M.: Stabilizing mechanisms in insect flight. Proc. Int. Study Conf. Current and future problems of acridology. London 1970Google Scholar
  83. Wilson, M.: Angular sensitivity of light and dark adapted locust retinula cells. J. comp. Physiol.97, 323–328 (1975a)Google Scholar
  84. Wilson, M.: Autonomous pigment movement in the radial pupil of locust ocelli. Nature (Lond.)258, 603–604 (1975b)Google Scholar
  85. Wolsky, A.: Optische Untersuchungen über die Bedeutung und Funktion der Insektenocellen. Z. vergl. Physiol.12, 783–787 (1930)Google Scholar
  86. Wolsky, A.: Weitere Beiträge zum Ocellenproblem. Die optischen Verhältnisse der Ocellen der Honigbiene (Apis mellifica L.). Z. vergl. Physiol.14, 385–389 (1931)Google Scholar

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© Springer-Verlag 1978

Authors and Affiliations

  • Martin Wilson
    • 1
  1. 1.Department of Neurobiology, Research School of Biological SciencesAustralian National UniversityCanberraAustralia

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