Journal of Comparative Physiology A

, Volume 175, Issue 3, pp 289–302 | Cite as

Did neural pooling for night vision lead to the evolution of neural superposition eyes?

  • D. -E. Nilsson
  • A. -I. Ro
Original Papers


Observations of the infrared deep pseudopupil, optical determinations of the corneal nodal point, and histological methods were used to relate the visual fields of individual rhabdomeres to the array of ommatidial optical axes in four insects with open rhabdoms: the tenebrionid beetle Zophobas morio, the earwig Forficula auricularia, the crane fly Tipula pruinosa, and the backswimmer Notonecta glauca.

The open rhabdoms of all four species have a central pair of rhabdomeres surrounded by six peripheral rhabdomeres. At night, a distal pigment aperture is fully open and the rhabdom receives light over an angle approximately six times the interommatidial angle. Different rhabdomeres within the same ommatidium do not share the same visual axis, and the visual fields of the peripheral rhabdomeres overlap the optical axes of several near-by ommatidia. During the day, the pigment aperture is considerably smaller, and all rhabdomeres share the same visual field of about two interommatidial angles, or less, depending on the degree of light adaptation. The pigment aperture serves two functions: (1) it allows the circadian rhythm to switch between the night and day sampling patterns, and (2) it works as a light driven pupil during the day.

Theoretical considerations suggest that, in the night eye, the peripheral retinula cells are involved in neural pooling in the lamina, with asymmetric pooling fields matching the visual fields of the rhabdomeres. Such a system provides high sensitivity for nocturnal vision, and the open rhabdom has the potential of feeding information into parallel spatial channels with different tradeoffs between resolution and sensitivity. Modification of this operational principle to suit a strictly diurnal life, makes the contractile pigment aperture superfluous, and decreasing angular sensitivities together with decreasing pooling fields lead to a neural superposition eye.

Key words

Compound eye Open rhabdom Neural superposition Visual ecology Evolution 



deep pseudopupil


large monopolar cell


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  1. Bedau K (1911) Das Facettenauge der Wasserwanzen. Z Zool 97: 417–456Google Scholar
  2. Brammer JD (1970) The ultrastructure of the compound eye of a mosquito Aedes aegypti L. J Exp Zool 175: 181–196Google Scholar
  3. Braitenberg V (1967) Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Exp Brain Res 3: 271–298Google Scholar
  4. Burton PR, Stockhammer KA (1969) Electron microscopic studies of the compound eye of the toadbug, Gelastocoris oculatus. J Morphol 127: 233–258Google Scholar
  5. Chu H, Norris DM, Carlson SD (1975) Ultrastructure of the compound eye of the diploid female beetle, Xyleborus ferrugineus. Cell Tissue Res 165: 23–36Google Scholar
  6. Dahmen H (1991) Eye specialisation in waterstriders: an adaptation to life in a flat world. J Comp Physiol A 169: 623–632Google Scholar
  7. Eckert M (1968) Hell-Dunkel Adaptation in aconen Appositionsaugen der Insekten. Zool Jb Physiol 74: 102–120Google Scholar
  8. Franceschini N, Kirschfeld K (1971) Les pénoménes de pseudopupille dans l'<1,167>il composé de Drosophila. Kybernetik 9: 159–182Google Scholar
  9. Galbraith W (1955) The optical measurement of depth. Q J Microsc Sci 96: 285–288Google Scholar
  10. Gokan N, Hosobuchi K (1979a) Fine structure of the compound eyes of Longicorn beetles (Coleoptera: Cerambycidae). Appl Entomol Zool 14: 12–27Google Scholar
  11. Gokan N, Hosobuchi K (1979b) Ultrastructure of the compound eye of the longicorn beetle Prionus insularis Motschulsky (Coleoptera: Cerambycidae). Kontyû 47: 105–116Google Scholar
  12. Götz KG (1965) Die optischen Übertragungseigenschaften der Komplexaugen von Drosophila. Kybernetik 2: 215–221Google Scholar
  13. Hanström B (1927) Über die Frage, ob funktionell verschiedene zapfen- und stäbchenartige Sehzellen im Komplexauge der Arthropoden vorkommen. Z Vergl Physiol 6: 566–597Google Scholar
  14. Hardie RC (1986) The photoreceptor array of the dipteran retina. Trends Neurosci 9: 419–423Google Scholar
  15. Horridge GA, Meinertzhagen IA (1970) The exact projection of the visual fields upon the first and second ganglia of the insect eye. Z Vergl Physiol 66: 369–378Google Scholar
  16. Horridge GA, Duniec J, Marcelja L (1981) A 24-hour cycle in single locust and mantis photoreceptors. J Exp Biol 91: 300–322Google Scholar
  17. Howard J, Snyder AW (1983) Transduction as a limitation on compound eye function and design. Proc R Soc Lond B 217: 287–307Google Scholar
  18. Ichikawa T, Tateda H (1980) Cellular patterns and spectral sensitivity of larval ocelli in the swallowtail butterfly Papilio. J Comp Physiol 139: 41–47Google Scholar
  19. Ichikawa T, Tateda H (1982) Receptive field of the stemmata in the swallowtail butterfly Papilio. J Comp Physiol 146: 191–199Google Scholar
  20. Ioannides AC, Horridge GA (1975) The organization of visual fields in the hemipteran acone eye. Proc R Soc Lond B 190: 373–391Google Scholar
  21. Kirschfeld K (1967) Die Projection der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. ExpBrain Res 3: 248–270Google Scholar
  22. Kuhn O (1926) Die Facettenaugen der Landwanzen und Zikaden. Z Morphol Ökol 5: 489–558Google Scholar
  23. Land MF (1981) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 471–592Google Scholar
  24. Laughlin SB (1984) The roles of parallel channels in early visual processing by the arthropod compound eye. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 457–481Google Scholar
  25. Laughlin SB, Osorio D (1989) Mechanisms for neural signal enhancement in the blowfly compound eye. J Exp Biol 144: 113–146Google Scholar
  26. Lin J-T (1993) Identification of photoreceptor locations in the compound eye of Coccinella septempunctata Linnaeus (Coleoptera, Coccinellidae) J Insect Physiol 39: 555–562Google Scholar
  27. McLean M, Horridge GA (1977) Structural changes in light- and dark-adapted compound eyes of the Australian earwig Labidura riparia truncata (Dermaptera). Tissue Cell 9: 653–666Google Scholar
  28. Meinertzhagen IA (1976) The organization of perpendicular fibre pathways in the insect optic lobe. Phil Trans R Soc Lond B 274: 555–594Google Scholar
  29. Meinertzhagen IA (1991) Evolution of the cellular organization of the compound eye and optic lobe. In: Cronly-Dillon JR, Gregory RL (eds) Vision and visual dysfunction, vol. 2, Evolution of the eye and visual system. Macmillan Press, London, pp341–363Google Scholar
  30. Melzer RR, Paulus HF (1991) Morphology of the visual system of Chaoborus crystallinus (Diptera, Chaoboridae). I. Larval compound eyes and stemmata. Zoomorphologie 110: 227–238Google Scholar
  31. Meyer-Rochow VB, Gokan N (1988) Functional aspects and eye organization of black and white morphs of the New Zealand beach beetle Chaerodes trachyscelides (Tenebrionidae). J Insect Physiol 34: 983–995Google Scholar
  32. Meyer-Rochow VB, Waldvogel H (1979) Visual behaviour and the structure of dark and light-adapted larval and adult eyes of the New Zealand glowworm Arachnocampa luminosa (Mycetophilidae: Diptera). J Insect Physiol 25: 601–613Google Scholar
  33. Müller J (1970) Feinbau und Dunkelanpassung der Komplexaugen von Rhodnius prolixus (Stal). Zool Jb Physiol 75: 111–133Google Scholar
  34. Nässel DR, Waterman TH (1979) Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J Comp Physiol 131: 205–216Google Scholar
  35. Nilsson D-E (1989) Optics and evolution of the compound eye. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin, pp 30–73Google Scholar
  36. Nilsson D-E, Land MF, Howard J (1988) Optics of the butterfly eye. J Comp Physiol A 162: 341–366Google Scholar
  37. O'Grady GE, McIver SB (1987) Fine structure of the compound eye of the black fly Simulium vittatum (Diptera: Simuliidae). Can J Zool 65: 1454–1469Google Scholar
  38. Ohly KP (1975) The neurons of the first synaptic region of the optic neuropil of the firefly, Phausius splendidula L. Coleoptera. Cell Tissue Res 158: 89–109Google Scholar
  39. Pick B (1977) Specific misalignments of rhabdomere visual axes in the neural superposition eye of dipteran flies. Biol Cybern 26: 215–224Google Scholar
  40. Ro A-I, Nilsson D-E (1993a) The circadian pupil rhythm in Tenebrio molitor, studied noninvasively. Naturwissenschaften 80: 186–189Google Scholar
  41. Ro A-I, Nilsson D-E (1993b) Sensitivity and dynamics of the pupil mechanism in two tenebrionid beetles. J Comp Physiol A 173: 455–462Google Scholar
  42. Ro A-I, Nilsson D-E (1994a) Circadian and light-dependent control of the pupil mechanism in tipulid flies. J Insect Physiol (in press)Google Scholar
  43. Ro A-I, Nilsson D-E (1994b) Pupil adjustments in the eye of the common backswimmer. J Exp Biol (in press)Google Scholar
  44. Schmitt M, Mischke, Wachmann E (1982) Phylogenetic and functional implications o the rhabdom pattern in the eyes of Chrysomeloidea (Coleoptera). Zoologica Scripta 11: 31–44Google Scholar
  45. Schneider L, Langer H (1969) Die Struktur des Rhabdoms im “Doppelauge” des Wasserläufers Gerris lacustris. Z Zellforsch 99: 538–559Google Scholar
  46. Schwind R (1980) Geometrical optics of the Notonecta eye: adaptations to optical environment and way of life. J Comp Physiol 140: 59–68Google Scholar
  47. Schwind R (1983) Zonation of the optical environment and zonation in the rhabdom structure within the eye of the backswimmer, Notonecta glauca. Cell Tissue Res 232: 53–63Google Scholar
  48. Schwind R, Schlecht P, Langer H (1984) Microspectrophotometric characterization and localization of three visual pigments in the compound eye of Notonecta glauca L. (Heteroptera). J Comp Physiol A 154: 341–346Google Scholar
  49. Seifert P, Wunderer H (1990) Hell- und Dunkeladaptation bei Dipteren — eine funktioneile Vorbindung zur Rhabdomentwicklung? Mitt Dtsch Ges Allg Angew Entomol 7: 487–491Google Scholar
  50. Shaw SR (1989) The retina-lamina pathway in insects, particularly Diptera, viewed from an evolutionary perspective. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin, pp 186–212Google Scholar
  51. Shaw SR (1990) The photoreceptor axon projections and its evolution in the neural superposition eye of some primitive brachyceran Diptera. Brain Behav Evol 1990: 107–125Google Scholar
  52. Shaw SR, Meinertzhagen IA (1986) Evolutionary progression at synaptic connections made by identified homologous neurones. Proc Natl Acad Sci USA 83: 7961–7965Google Scholar
  53. Shaw SR, Moore D (1989) Evolutionary remodeling in a visual system through extensive changes in the synaptic connectivity of homologous neurons. Visual Neurosci 3: 405–410Google Scholar
  54. Shelton PMJ, Lawrence PA (1974) Structure and development of ommatidia in Oncopeltus fasciatus. J Embryol Exp Morphol 32: 337–353Google Scholar
  55. Snyder AW (1977) Acuity of compound eyes: Physical limitations and design. J Comp Physiol 116: 161–182Google Scholar
  56. Snyder AW (1979) Physics of vision in compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin Heidelberg New York, pp 225–313Google Scholar
  57. Snyder AW, Menzel R, Laughlin SB (1973) Structure and function of the fused rhabdom. J Comp Physiol 87: 99–135Google Scholar
  58. Snyder AW, Stavenga DG, Laughlin SB (1977) Spatial information capacity of compound eyes. J Comp Physiol 116: 183–207Google Scholar
  59. Stavenga DG (1975) The neural superposition eye and its optical demands. J Comp Physiol 102: 297–304Google Scholar
  60. Stavenga DG (1979) Pseudopupils of compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin Heidelberg New York, pp 357–439Google Scholar
  61. Strausfeld NJ, Blest AD (1970) Golgi studies on insects. Part I. The optic lobe of Lepidoptera. Phil Trans R Soc Lond B 258: 81–134Google Scholar
  62. Strausfeld NJ, Nässel DR (1981) Neuroarchitectures serving compound eyes of Crustacea and insects. In: Autrum HJ (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 1–132Google Scholar
  63. Tuurala O (1963) Bau und photomechanische Erscheinungen im Auge einiger Chironomiden (Dipt.). Ann Entomol Fenn 29: 209–217Google Scholar
  64. Wachmann E (1977) Vergleichende Analyse der feinstrukturellen Organisation offener Rhabdome in den Augen der Cucujiformia (Insecta, Coleoptera), unter besonderer Berücksichtigung der Chrysomelidae. Zoomorphologie 88: 95–131Google Scholar
  65. Wachmann E (1979) Untesuchungen zur Feinstruktur der Augen von Bockkäfern (Coleoptera, Cerambycidae). Zoomorphologie 92: 19–48Google Scholar
  66. Walcott B (1971) Cell movement on light adaptation in the retina of Lethocerus (Belostomatidae, Hemiptera). Z Vergl Physiol 74: 1–16Google Scholar
  67. Warrant EJ (1993) Can neural pooling help insects see at night? Proc IEEE Int Conf Syst Man Cybern, vol 3. Imprimerie Artésienne, LiévinGoogle Scholar
  68. Wehner R (1975) Pattern recognition. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 75–113Google Scholar
  69. Williams DS (1980) Organisation of the compound eye of a tipulid fly during the day and night. Zoomorphologie 95: 85–104Google Scholar
  70. Williams DS (1983) Changes of photoreceptor performance associated with the daily turnover of photoreceptor membrane in the locust. J Comp Physiol 150: 509–519Google Scholar
  71. Williams DS, Blest AD (1980) Extracellular shedding of photoreceptor membrane in the open rhabdom of a tipulid fly. Cell Tissue Res 205: 423–438Google Scholar
  72. Wolburg-Buchholz K (1979) The organization of the lamina ganglionaris of the hemipteran insects, Notonecta glauca, Corixa punctata and Gerris lacustris. Cell Tissue Res 197: 39–59PubMedGoogle Scholar
  73. Zeil J (1979) A new kind of neural superposition eye: the compound eye of male Bibionidae. Nature 278: 249–250Google Scholar
  74. Zeil J (1983) Sexual dimorphism in the visual system of flies: The compound eyes and neural superposition in Bibionidae (Diptera). J Comp Physiol 150: 379–393Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • D. -E. Nilsson
    • 1
  • A. -I. Ro
    • 1
  1. 1.Department of ZoologyUniversity of LundLundSweden

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