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Longterm dark induced fine structural changes in crayfish photoreceptor membrane

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Summary

  1. 1.

    Fine structural effects of longterm continuous darkness (2–16 weeks) have been quantitatively measured in five rhabdom parameters of adult crayfish (Procambarus) using transmission (Figs. 3–6) and freeze fracture (Figs. 13–15) electron micrographs. The most striking modifications took place during the first four weeks.

  2. 2.

    During the first two weeks in darkness four changes occurred: a) the diameter of rhabdom microvilli increased significantly (Figs. 9, 10), b) the diameter of particles (one or more rhodopsin molecules) visualized on the protoplasmic face of the receptor membrane by freeze fracture (Figs. 13–15) decreased significantly, whereas c) their number increased (Fig. 16) and d) lysosome related bodies near the rhabdom (Figs. 3, 4) in all five retinular regions studied strongly decreased in number (Fig. 12).

  3. 3.

    During weeks 3 and 4 in darkness two further changes occurred: a) the normally regular microvillus pattern of the photoreceptor membrane (Figs. 1, 2) was significantly disrupted and b) the number of membrane particles then fell to about half their initial count (Fig. 16) except in retinular cell eight where they maintained control levels for up to two months in the dark.

  4. 4.

    Most of these effects of prolonged darkness have clear functional implications. Disruption of microvillus pattern and sustained decrease in visual pigment concentration after more than two weeks without light reflect deterioration in vision. Alterations in microvillus diameters and lysosome density imply changes in the membrane turnover steady state resulting from protracted darkness. The data demonstrate that normal photoreceptor membrane could not be maintained in this eye for long in the absence of light.

  5. 5.

    The dark-induced disorganization of microvillus regularity confirms the earlier, disputed demonstration but also shows regional differences in susceptibility which might explain different conclusions drawn from local samples.

  6. 6.

    New distinctive features of retinular cell eight were found in its minimal sensitivity to microvillus disruption compared with the seven regular retinular cells and its maintenance of control densities of membrane particles despite two months continuous darkness.

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Abbreviations

i :

irregularity index

mvl :

microvillus(i)

References

  • Ball, E.E.: Fine structure of the compound eyes of the midwater amphipodPhronima in relation to behavior and habitat. Tissue Cell9, 521–536 (1977)

    Google Scholar 

  • Barnes, S. N., Goldsmith, T. H.: Dark adaptation, sensitivity, and rhodopsin level in the eye of the lobster,Homarus. J. Comp. Physiol.120, 143–159 (1977)

    Google Scholar 

  • Bedini, C., Ferrero, E., Lanfranchi, A.: Fine structural changes induced by circadian light-dark cycles in photoreceptors of Dalyelliidae (Turbellaria: Rhabdocoela). J. Ultrastruct. Res.58, 66–77 (1977)

    Google Scholar 

  • Besharse, J.C., Brandon, R.A.: Effects of continuous light and darkness on the eyes of the troglobitic salamanderTyphlotriton spelaeus. J. Morphol.149, 527–546 (1976)

    Google Scholar 

  • Besharse, J.C., Hollyfield, J.G.: Ultrastructural changes during degeneration of photoreceptors and pigment epithelium in the Ozark cave salamander. J. Ultrastruct. Res.59, 31–43 (1977)

    Google Scholar 

  • Besharse, J.C., Hollyfield, J.G., Rayborn, M.E.: Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relation to light. J. Cell Biol.75, 507–526 (1977)

    Google Scholar 

  • Blest, A.D.: The rapid synthesis and destruction of photoreceptor membrane by a dinopid spider: a daily cycle. Proc. R. Soc. London B200, 463–483 (1978)

    Google Scholar 

  • Blest, A.D., Day, W.A.: The rhabdomere organization of some nocturnal Pisaurid spiders in light and darkness. Philos. Trans. R. Soc. London B283, 1–23 (1978)

    Google Scholar 

  • Blest, A.D., Land, M.F.: The physiological optics ofDinopis subrufus L. Koch: a fish-lens in a spider. Proc. R. Soc. London B196, 197–222 (1977)

    Google Scholar 

  • Boschek, C.B., Hamdorf, K.: Rhodopsin particles in the photoreceptor membrane of an insect. Z. Naturforsch.31 c, 763 (1976)

    Google Scholar 

  • Brammer, J.D., Clarin, B.: Changes in volume of the rhabdom in the compound eye ofAedes aegypti L. J. Exp. Zool.195, 33–40 (1976)

    Google Scholar 

  • Brammer, J.D., White, R.H.: Vitamin A deficiency: effect on mosquito eye ultrastructure. Science163, 821–823 (1969)

    Google Scholar 

  • Brandenburger, J.L.: Cytochemical localization of acid phospha-tase in regenerated and dark-adapted eyes of a snail,Helix aspersa. Cell Tiss. Res.184, 301–313 (1977)

    Google Scholar 

  • Brandenburger, J.L., Eakin, R.M., Reed, C.T.: Effects of light- and dark-adaptation on the photic microvilli and photic vesicles of the pulmonate snailHelix aspersa. Vision Res.16, 1205–1210 (1976)

    Google Scholar 

  • Bruno, M., Barnes, S.N., Goldsmith, T.H.: The visual pigment and visual cycles of the lobster,Homarus. J. Comp. Physiol.120, 123–142 (1977)

    Google Scholar 

  • Carlson, S., Gemne, G., Robbins, W.: Ultrastructure of photoreceptor cells in a vitamin A deficient moth (Manduca sexta). Experientia25, 175–177 (1969)

    Google Scholar 

  • Carpenter, K.S., Morita, M., Best, J.B.: Ultrastructure of the photoreceptor of the planarianDugesia dorotocephala. II. Changes induced by darkness and light. Cytobiologie8, 320–338 (1974)

    Google Scholar 

  • Chow, K.L.: Neuronal changes in the visual system following deprivation. In: Handbook of sensory physiology, Vol. VII/3A. Jung, R. (ed.), pp. 607–627. Berlin, Heidelberg, New York: Springer 1973

    Google Scholar 

  • Chow, K.L., Riesen, A.H., Newell, F.W.: Regeneration of retinal ganglion cells in infant chimpanzees reared in darkness. J. Comp. Neurol.107, 27–42 (1957)

    Google Scholar 

  • Corless, J.M., Cobbs, W.H., III, Costello, M.J., Robertson, J.D.: On the asymmetry of frog retinal rod outer segment disk membrane. Exp. Eye Res.23, 295–324 (1976)

    Google Scholar 

  • Cosens, D.: The effect of short wavelength light on retinula cell structure in white-eyeDrosophila. J. Insect Physiol.22, 497–504 (1976)

    Google Scholar 

  • Dowling, J.E., Wald, G.: The biological function of vitamin A acid. Proc. Natl. Acad. Sci. (Wash.)46, 587–608 (1960)

    Google Scholar 

  • Durand, J.P.: Ocular development and involution in the European cave salamander,Proteus anguinus Laurenti. Biol. Bull.151, 450–466 (1976)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Ultrastructural effects of dark-adaptation on eyes of a snail,Helix aspersa. J. Exp. Zool.187, 127–133 (1974)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Retinal differences between light-tolerant and light-avoiding slugs (Mollusca: Pulmonata). J. Ultrastruct. Res.53, 382–394 (1975)

    Google Scholar 

  • Ebrey, T.G., Honig, B.: Molecular aspects of photoreceptor function. Q. Rev. Biophys.8, 129–184 (1975)

    Google Scholar 

  • Eguchi, E.: The structure of rhabdom and action potentials of single retinula cells in crayfish. 25 pp. Ph.D. Thesis, Kyushu University, Japan (1964)

    Google Scholar 

  • E+guchi, E.: Rhabdom structure and receptor potentials in single crayfish retinular cells. J. Cell. Comp. Physiol.66, 411–429 (1965)

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Fine structure patterns in crustacean rhabdoms. In: The functional organization of the compound eye. Bernhard, C.G. (ed.), pp. 105–124. Oxford: Pergamon Press 1966

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Changes in retinal fine structure induced in the crabLibinia by light and dark adaptation. Z. Zellforsch.79, 209–229 (1967)

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Cellular basis for polarized light perception in the spider crab,Libinia. Z. Zellforsch.84, 87–101 (1968)

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membrane. Cell Tiss. Res.169, 419–434 (1976)

    Google Scholar 

  • Eguchi, E., Waterman, T.H., Akiyama, J.: Localization of the violet and yellow receptor cells in the crayfish retinula. J. Gen. Physiol.62, 355–374 (1973)

    Google Scholar 

  • Elofsson, R., Hallberg, E.: Compound eyes of some deep-sea and fiord mysid crustaceans. Acta Zool. (Stockh.)58, 169–177 (1977)

    Google Scholar 

  • Fernández, H.R., Nickel, E.E.: Ultrastructural and molecular characteristics of crayfish photoreceptor membranes. J. Cell Biol.69, 721–732 (1976)

    Google Scholar 

  • Goldsmith, T.H., Barker, R.J., Cohen, C.F.: Sensitivity of visual receptors of carotenoid-depleted flies: a vitamin A deficiency in an invertebrate. Science146, 65–67 (1964)

    Google Scholar 

  • Goldsmith, T.H., Wehner, R.: Restrictions of rotational and translational diffusion of pigment in the membranes of a rhabdo-meric photoreceptor. J. Gen. Physiol.70, 453–490 (1977)

    Google Scholar 

  • Harris, W.A., Ready, D.F., Lipson, E.D., Hudspeth, A.J., Stark, W.S.: Vitamin A deprivation andDrosophila photopigments. Nature266, 648–650 (1977)

    Google Scholar 

  • Hobbs, H.H., Jr., Hobbs, H.H., III, Daniel, M.A.: A review of the troglobitic decapod crustaceans of the Americas. Smithson. Contrib. Zool.244, 1–183 (1977)

    Google Scholar 

  • Hollyfield, J.G., Besharse, J.C., Rayborn, M.E.: Turnover of rod photoreceptor outer segments. I. Membrane addition and loss in relation to temperature. J. Cell Biol.75, 490–506 (1977)

    Google Scholar 

  • Holmberg, K.: The cyclostome retina. In: Handbook of sensory physiology, Vol. VII/5. Crescitelli, F. (ed.), pp. 47–66. Berlin, Heidelberg, New York: Springer 1977

    Google Scholar 

  • Holtzman, E., Schacher, S., Evans, J., Teichberg, S.: Origin and fate of the membranes of secretion granules and synaptic vesicles: membrane circulation in neurons, gland cells and retinal photoreceptors. In: The synthesis, assembly and turnover of cell surface components. Poste, G., Nicolson, G.E. (eds.), pp. 165–246. Amsterdam: Elsevier/North Holland Biomedical Press 1977

    Google Scholar 

  • Hughes, A.: The topography of vision in mammals of contrasting life styles: comparative optical and retinal organisation. In: Handbook of sensory physiology, Vol. VII/5. Crescitelli, F. (ed.), pp. 613–756. Berlin, Heidelberg, New York: Springer 1977

    Google Scholar 

  • Itaya, S.K.: Rhabdom changes in the shrimpPalaemonetes. Cell Tiss. Res.166, 256–273 (1976)

    Google Scholar 

  • Jan, L.Y., Revel, J.-P.: Ultrastructural localization of rhodopsin in the vertebrate retina. J. Cell Biol.62, 257–273 (1964)

    Google Scholar 

  • Kong, K.-E., Goldsmith, T.H.: Photosensitivity of retinular cells in white-eyed crayfish (Procambarus clarkii). J. Comp. Physiol.122, 273–288 (1977)

    Google Scholar 

  • Krebs, W., Kühn, H.: Structure of isolated bovine rod outer segment membranes. Exp. Eye Res.25, 511–526 (1977)

    Google Scholar 

  • Kuwabara, T., Gorn, R.A.: Retinal damage by visible light. An electron microscopic study. Arch. Ophthalmol.79, 69–78 (1968)

    Google Scholar 

  • LaVail, M.M.: Rod outer segment disk shedding in rat retina; relationship to cyclic lighting. Science194, 1071–1073 (1976a)

    Google Scholar 

  • LaVail, M.M.: Rod outer segment disc shedding in relation to cyclic lighting. Exp. Eye Res.23, 277–280 (1976b)

    Google Scholar 

  • Locket, N.A.: Adaptations to the deep-sea environment. In: Handbook of sensory physiology, Vol. VII/5. Crescitelli, F. (ed.), pp. 68–192. Berlin, Heidelberg, New York: Springer 1977

    Google Scholar 

  • Loew, E.R.: Light, and photoreceptor degeneration in the Norway lobster,Nephrops norvegicus (E). Proc. R. Soc. London B193. 31–44 (1976)

    Google Scholar 

  • Munz, F. W., McFarland, W.N.: Evolutionary adaptations of fishes to the photic environment. In: Handbook of sensory physiology, Vol. VII/5. Crescitelli, F. (ed.), pp. 193–274. Berlin, Heidelberg, New York: Springer 1977

    Google Scholar 

  • Nässel, D.R., Waterman, T.H.: Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J. Comp. Physiol.131, 205–216 (1979)

    Google Scholar 

  • Nemanic, P.: Fine structure of the compound eye ofPorcellio scaber in light and dark adaptation. Tissue Cell7, 453–468 (1975)

    Google Scholar 

  • Nickel, E., Menzel, R.: Insect UV- and green-photoreceptor membranes studied by the freeze-etch technique. Cell Tiss. Res.175, 357–368 (1976)

    Google Scholar 

  • Noell, W.K., Walker, V.S., Kang, B.S., Berman, S.: Retinal damage by light in rats. Invest. Ophthalmol.5, 450–473 (1966)

    Google Scholar 

  • O'Day, W.T., Young, R.W.: Rhythmic daily shedding of outer-segment membranes by visual cells in the goldfish. J. Cell Biol.76, 593–604 (1978)

    Google Scholar 

  • Pecci Saavedra, J., Pellegrino de Iraldi, A.: Retinal alterations induced by continuous light in immature rats. I. Fine structure and electroretinography. Cell Tiss. Res.166, 202–211 (1976)

    Google Scholar 

  • Remé, C.E., Young, R.W.: The effects of hibernation on cone visual cells in the ground squirrel. Invest. Ophthalmol.16, 815–840 (1977)

    Google Scholar 

  • Roach, J.E.M., Wiersma, C.A.G.: Differentiation and degeneration of crayfish photoreceptors in darkness. Cell Tiss. Res.153, 137–144 (1974)

    Google Scholar 

  • Robison, W.G. Jr., Kuwabara, T.: Eight-induced alterations of retinal pigment epithelium in black, albino and beige mice. Exp. Eye Res.22, 549–557 (1976)

    Google Scholar 

  • Röhlich, P.: Fine structural changes induced in photoreceptors by light and prolonged darkness. In: Symposium on neurobiol-ogy of invertebrates, Tihany, Hungary, 1967. Salanki, J. (ed.), pp. 95–109. New York: Plenum Press 1968

    Google Scholar 

  • Röhlich, P.: Differentiation and regulation in invertebrate photoreceptors. In International cell biology. Brinkley, B.R., Porter, K.R. (eds.), pp. 618–625. New York: Rockefeller University Press 1977

    Google Scholar 

  • Röhlich, P., Tar, E.: The effect of prolonged light-deprivation on the fine structure of planarian photoreceptors. Z. Zellforsch.90, 507–518 (1968)

    Google Scholar 

  • Tomita, T.: Electrical activity of vertebrate photoreceptors. Q. Rev. Biophys.3, 179–222 (1970)

    Google Scholar 

  • Tomita, T.: Electrophysiological studies of retinal cell function. Invest. Ophthalmol.15, 171–187 (1976)

    Google Scholar 

  • Vandel, A.: Biospeleology. 524 pp. Oxford: Pergamon Press 1965

    Google Scholar 

  • Waterman, T.H.: Expectation and achievement in comparative physiology. J. Exp. Zool.194, 309–343 (1975)

    Google Scholar 

  • Waterman, T.H.: Polarization sensitivity. In: Handbook of sensory physiology, Vol. VII/6B. Autrum, H. (ed.). Berlin, Heidelberg, New York: Springer (in press) (1979)

    Google Scholar 

  • White, R.H.: The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. II. The rhabdom. J. Exp. Zool.166, 405–426 (1967)

    Google Scholar 

  • 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 

  • 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 

  • Wiesel, T.N., Hubel, D.H.: Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J. Neurophysiol.26, 978–993 (1963)

    Google Scholar 

  • Yamamoto, M., Yoshida, M.: Fine structure of the ocelli of a synaptid holothurianOpheodesoma spectabilis and the effects of light and darkness. Zoomorphologie90, 1–17 (1978)

    Google Scholar 

  • Young, R.W.: Visual cells and the concept of renewal. Invest. Ophthalmol.15, 700–725 (1976)

    Google Scholar 

  • Young, R.W.: The daily rhythm of shedding and degradation of cone outer segment membranes in the lizard retina. J. Ultra-struct. Res.61, 172–185 (1977)

    Google Scholar 

  • Young, R.W.: The daily rhythm of shedding and degradation of rod and cone outer segment membranes in the chick retina. Invest. Ophthalmol.17, 105–116 (1978)

    Google Scholar 

  • Zimmerman, W.F., Goldsmith, T.H.: Photosensitivity of the circadian rhythm and of visual receptors in carotenoid depletedDrosophila. Science171, 1167–1169 (1971)

    Google Scholar 

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  1. Eisuke Eguchi

    Present address: Department of Biology, Yokohama City University, Mutsuura, Kanazawa-ku, 236, Yokohama, Japan

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  1. 610 KBT, Department of Biology, Yale University, 06520, New Haven, Connecticut, USA

    Eisuke Eguchi & Talbot H. Waterman

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  1. Eisuke Eguchi
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Supported by grants from the U.S. National Institutes of Health (EY00405) and from the National Geographic Society Committee on Research

We are grateful to Professor Vincent Marchesi of the Yale Pathology Department for generously sharing the freeze-fracture facility in his laboratory.

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Eguchi, E., Waterman, T.H. Longterm dark induced fine structural changes in crayfish photoreceptor membrane. J. Comp. Physiol. 131, 191–203 (1979). https://doi.org/10.1007/BF00610428

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