Journal of comparative physiology

, Volume 107, Issue 1, pp 77–96 | Cite as

The effect of light-dark adaptation on the ultrastructure ofLimulus lateral eye retinular cells

  • Mildred Behrens
  • Wolf Krebs


The fine structure of retinular cells within lateral eyes ofLimulus polyphemus which had been dark or light adapted for 12 h in vivo was studied via electron microscopy. The ommatidium to ommatidium and retinular cell to retinular cell variability observed in light microscope studies was confirmed. The rhabdomeric microvilli were longer and narrower, the area of contiguous microvillar membranes greater, the endoplasmic reticulum less abundant and the mitochondrial granules (? calcium containing) more numerous in well dark adapted than in well light adapted retinular cells (Figs. 1, 3, 4, 7, 8) and membrane whorls or “vacuoles” were present in the peripheral cytoplasm of very well light adapted retinular cells (Fig. 6). Phagocytotic vesicles, multivesicular bodies and lysosomes were present in the interrhabdomeral cytoplasm of partially light adapted retinular cells (Figs. 1, 2, 3, 10). The number of retinular cell microvilli in contact with the eccentric cell dendrite was smaller in very well light adapted than in well dark adapted ommatidia (Fig. 9). The possible functional significance of these light-dependent structural changes is discussed.


Calcium Endoplasmic Reticulum Cell Dendrite Light Microscope Fine Structure 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Behbehani, M., Srebro, R.: Discrete waves and phototransduction in voltage-clamped ventral photoreceptors. J. gen. Physiol.64, 186–200 (1974)Google Scholar
  2. Behrens, M.: Photomechanical changes in the ommatidia of theLimulus lateral eye during light and dark adaptation. J. comp. Physiol.89, 45–57 (1974)Google Scholar
  3. Borle, A.B.: Cyclic AMP stimulation of calcium efflux from kidney, liver and heart mitochondria. J. Membrane Biol.16, 221–236 (1974)Google Scholar
  4. Brammer, J.D., White, R.H.: Vitamin A deficiency: Effect on mosquito eye ultrastructure. Science163, 821–823 (1969)Google Scholar
  5. Brandenburger, J.L., Eakin, R.M.: Pathway of incorporation of vitamin A3H2 into photoreceptors of a snail,Helix aspersa. Vision Res.10, 639–653 (1970)Google Scholar
  6. Brown, J.E., Blinks, J.R.: Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J. gen. Physiol.64, 643–665 (1974)Google Scholar
  7. Burnel, M., Mahler, H.R., Moore, W.J.: Protein synthesis in visual cells ofLimulus. J. Neurochem.17, 1493–1499 (1970)Google Scholar
  8. Carlson, S.D., Gemne, G., Robbins, W.E.: Ultrastructure of photoreceptor cells in a vitamin A-deficient moth (Manduca sexta). Experientia (Basel)25, 175–177 (1969)Google Scholar
  9. De Mello, W.C.: Effect of intracellular injection of calcium and strontium on cell communication in heart. J. Physiol. (Lond.)250, 231–245 (1975)Google Scholar
  10. Dowling, J.E.: Discrete potentials in the dark-adapted eye of the crabLimulus. Nature (Lond.)217, 28–31 (1968)Google Scholar
  11. De Duve, C., Wattiaux, R.: Functions of lysosomes. Ann. Rev. Physiol.28, 435–492 (1966)Google Scholar
  12. Eguchi, E., Naka, K., Kuwabara, M.: The development of the rhabdom and the appearance of the electrical response in the insect eye. J. gen. Physiol.46, 143–157 (1962)Google Scholar
  13. Fahrenbach, W.H.: The fine structure of a nauplius eye. Z. Zellforsch.62, 182–197 (1964)Google Scholar
  14. Fahrenbach, W.H.: The morphology of the eyes ofLimulus. II. Ommatidia of the compound eye. Z. Zellforsch.93, 451–483 (1969)Google Scholar
  15. Fahrenbach, W.H.: The visual system of the horseshoe crabLimulus polyphemus. Inter. Rev. Cytol.41, 285–349 (1975)Google Scholar
  16. Fein, A., Lisman, J.: Localized desensitization ofLimulus photoreceptors produced by light or intracellular calcium ion injection. Science187, 1094–1096 (1975)Google Scholar
  17. Gribakin, F.G.: Functional morphology of the compound eye of the bee. In: The compound eye and vision of insects (ed. G.A. Horridge). Oxford: Clarendon Press 1975Google Scholar
  18. Hafner, G.S.: H3-leucine uptake and distribution in the retinular cells of the crayfish retina, (abstract). Spring Meeting of The Association for Research in Vision and Ophthalmology; Sarasota, Florida (1975)Google Scholar
  19. Horridge, G.A., Barnard, P.B.T.: Movement of palisade in locust retinula cells when illuminated. Quart. J. micr. Sci.106, 131–135 (1965)Google Scholar
  20. Hwang, K.M., Yang, L.C., Carrico, C.K., Schulz, R.A., Schenkman, J.B., Sartorelli, A.C.: Production of membrane whorls in rat liver by some inhibitors of protein synthesis. J. Cell Biol.62, 20–31 (1974)Google Scholar
  21. Kaplan, E.: Properties of visual cells in the lateral eye ofLimulus in situ. Special Report LSC-S-12, Laboratory of Sensory Communication, Syracuse University, Syracuse, New York (1973)Google Scholar
  22. Krischer, C.: On the mechanism of electric response of the photoreceptors of the barnacle and other animals. Z. Naturforsch.27, 409–413 (1972)Google Scholar
  23. Lasansky, A.: Cell junctions in ommatidia ofLimulus. J. Cell Biol.33, 365–383 (1967)Google Scholar
  24. Lehninger, A.L., Carafoli, E., Rossi, C.: Energy-linked ion movements in mitochondrial systems. In: Advances in enzymology, Vol. 29, (ed. F.F. Nord). New York: Interscience Publishers, Wiley and Sons 1967Google Scholar
  25. Levi-Setti, R., Park, D.A., Winston, R.: The corneal cones ofLimulus as optimized light concentrators. Nature (Lond.)253, 115–116 (1975)Google Scholar
  26. Miller, W.H., Morphology, of the ommatidia of the compound eye ofLimulus. J. biophys. biochem. Cytol.3, 421–428 (1957)Google Scholar
  27. Miller, W.H., Cawthon, D.F.: Pigment granule movement inLimulus photoreceptors. Invest. Ophthal.13, 401–405 (1974)Google Scholar
  28. Novikoff, A.B.: Lysosomes: A personal account. In: Lysosomes and storage diseases (eds. H.G. Hers, F. van Hoff). New York: Academic Press 1973Google Scholar
  29. Ong, J.E.: The micromorphology of the nauplius eye of the estuarine calanoid copepod,Sulcanus conflictus Nicholls (Crustacea). Tissue & Cell2, 589–610 (1970)Google Scholar
  30. Reynolds, E.S.: Liver parenchymal cell injury. III. The nature of calcium-associated electron-opaque masses in rat liver mitochondria following poisoning with carbon tetrachloride. J. Cell Biol.25, 53–75 (1965)Google Scholar
  31. Rose, B., Loewenstein, W.R.: Permeability of cell junction depends on local cytoplasmic calcium activity. Nature (Lond.)254, 250–252 (1975)Google Scholar
  32. Shaw, S.R.: Interreceptor coupling in ommatidia of drone honeybee and locust compound eyes. Vision Res.9, 999–1029 (1969)Google Scholar
  33. Smith, T.G., Baumann, F.: The functional organization within the ommatidium of the lateral eye ofLimulus. In: Progress in brain research. Vol. 31, Mechanisms of synaptic transmission. (eds. K. Akert, P.G. Waser). Amsterdam: Elsevier Publishing Co. 1969Google Scholar
  34. Snyder, A.W.: Optical properties of invertebrate photoreceptors. In: The Compound eye and vision of insects (ed. G.A. Horridge). Oxford: Clarendon Press 1975Google Scholar
  35. Snyder, A.W., Menzel, R., Laughlin, S.B.: Structure and function of the fused rhabdom. J. comp. Physiol.87, 99–135 (1973)Google Scholar
  36. Snyder, A.W., Miller, W.H.: Fly colour vision. Vision Res.12, 1389–1396 (1972)Google Scholar
  37. Srebro, R., Behbehani, M.: Light adaptation of discrete waves in theLimulus photoreceptor. J. gen. Physiol.60, 86–101 (1972)Google Scholar
  38. White, R.H.: The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. III. Multivesicular bodies and protein uptake. J. exp. Zool.169, 261–278 (1968)Google Scholar
  39. White, R.H., Lord, E.: Diminution and enlargement of the mosquito rhabdom in light and darkness. J. gen. Physiol.65, 583–598 (1975)Google Scholar
  40. Walcott, B.: Anatomical changes during light-adaptation in insect compound eye. In: The compound eye and vision of insects (ed. G.A. Horridge). Oxford: Clarendon Press 1975Google Scholar
  41. Yamamoto, T., Tasaki, K.. Sugawara, Y., Tonosaki, A.: Fine structure of the octopus retina. J. Cell Biol.25, 345–359 (1965)Google Scholar
  42. Young, R.W.: Biogenesis and renewal of visual cell outer segment membranes. Exp. Eye Res.18, 215–223 (1974)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • Mildred Behrens
    • 1
    • 3
  • Wolf Krebs
    • 2
  1. 1.The Masonic Medical Research LaboratoryUticaUSA
  2. 2.Institut für Neurobiologie, KernforschungsanlageJülichFederal Republic of Germany
  3. 3.Institut für Neurobiologie, KFAJülichFederal Republic of Germany

Personalised recommendations