Summary
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.
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References
Behbehani, M., Srebro, R.: Discrete waves and phototransduction in voltage-clamped ventral photoreceptors. J. gen. Physiol.64, 186–200 (1974)
Behrens, M.: Photomechanical changes in the ommatidia of theLimulus lateral eye during light and dark adaptation. J. comp. Physiol.89, 45–57 (1974)
Borle, A.B.: Cyclic AMP stimulation of calcium efflux from kidney, liver and heart mitochondria. J. Membrane Biol.16, 221–236 (1974)
Brammer, J.D., White, R.H.: Vitamin A deficiency: Effect on mosquito eye ultrastructure. Science163, 821–823 (1969)
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)
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)
Burnel, M., Mahler, H.R., Moore, W.J.: Protein synthesis in visual cells ofLimulus. J. Neurochem.17, 1493–1499 (1970)
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)
De Mello, W.C.: Effect of intracellular injection of calcium and strontium on cell communication in heart. J. Physiol. (Lond.)250, 231–245 (1975)
Dowling, J.E.: Discrete potentials in the dark-adapted eye of the crabLimulus. Nature (Lond.)217, 28–31 (1968)
De Duve, C., Wattiaux, R.: Functions of lysosomes. Ann. Rev. Physiol.28, 435–492 (1966)
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)
Fahrenbach, W.H.: The fine structure of a nauplius eye. Z. Zellforsch.62, 182–197 (1964)
Fahrenbach, W.H.: The morphology of the eyes ofLimulus. II. Ommatidia of the compound eye. Z. Zellforsch.93, 451–483 (1969)
Fahrenbach, W.H.: The visual system of the horseshoe crabLimulus polyphemus. Inter. Rev. Cytol.41, 285–349 (1975)
Fein, A., Lisman, J.: Localized desensitization ofLimulus photoreceptors produced by light or intracellular calcium ion injection. Science187, 1094–1096 (1975)
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 1975
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)
Horridge, G.A., Barnard, P.B.T.: Movement of palisade in locust retinula cells when illuminated. Quart. J. micr. Sci.106, 131–135 (1965)
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)
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)
Krischer, C.: On the mechanism of electric response of the photoreceptors of the barnacle and other animals. Z. Naturforsch.27, 409–413 (1972)
Lasansky, A.: Cell junctions in ommatidia ofLimulus. J. Cell Biol.33, 365–383 (1967)
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 1967
Levi-Setti, R., Park, D.A., Winston, R.: The corneal cones ofLimulus as optimized light concentrators. Nature (Lond.)253, 115–116 (1975)
Miller, W.H., Morphology, of the ommatidia of the compound eye ofLimulus. J. biophys. biochem. Cytol.3, 421–428 (1957)
Miller, W.H., Cawthon, D.F.: Pigment granule movement inLimulus photoreceptors. Invest. Ophthal.13, 401–405 (1974)
Novikoff, A.B.: Lysosomes: A personal account. In: Lysosomes and storage diseases (eds. H.G. Hers, F. van Hoff). New York: Academic Press 1973
Ong, J.E.: The micromorphology of the nauplius eye of the estuarine calanoid copepod,Sulcanus conflictus Nicholls (Crustacea). Tissue & Cell2, 589–610 (1970)
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)
Rose, B., Loewenstein, W.R.: Permeability of cell junction depends on local cytoplasmic calcium activity. Nature (Lond.)254, 250–252 (1975)
Shaw, S.R.: Interreceptor coupling in ommatidia of drone honeybee and locust compound eyes. Vision Res.9, 999–1029 (1969)
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. 1969
Snyder, A.W.: Optical properties of invertebrate photoreceptors. In: The Compound eye and vision of insects (ed. G.A. Horridge). Oxford: Clarendon Press 1975
Snyder, A.W., Menzel, R., Laughlin, S.B.: Structure and function of the fused rhabdom. J. comp. Physiol.87, 99–135 (1973)
Snyder, A.W., Miller, W.H.: Fly colour vision. Vision Res.12, 1389–1396 (1972)
Srebro, R., Behbehani, M.: Light adaptation of discrete waves in theLimulus photoreceptor. J. gen. Physiol.60, 86–101 (1972)
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)
White, R.H., Lord, E.: Diminution and enlargement of the mosquito rhabdom in light and darkness. J. gen. Physiol.65, 583–598 (1975)
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 1975
Yamamoto, T., Tasaki, K.. Sugawara, Y., Tonosaki, A.: Fine structure of the octopus retina. J. Cell Biol.25, 345–359 (1965)
Young, R.W.: Biogenesis and renewal of visual cell outer segment membranes. Exp. Eye Res.18, 215–223 (1974)
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This investigation was supported in part by Grant 2 RO1 EY 00236 National Eye Institute, National Institutes of Health
Member of the SFB 160 of the Deutsche Forschungsgemeinschaft
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Behrens, M., Krebs, W. The effect of light-dark adaptation on the ultrastructure ofLimulus lateral eye retinular cells. J. Comp. Physiol. 107, 77–96 (1976). https://doi.org/10.1007/BF00663920
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DOI: https://doi.org/10.1007/BF00663920