Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-13T07:44:48.923Z Has data issue: false hasContentIssue false
  • English
  • Français

Movement of retinal along cone and rod photoreceptors

Published online by Cambridge University Press:  02 June 2009

Jing Jin ,
Gregor J. Jones  and
M. Carter Cornwall
Jing Jin
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
Gregor J. Jones
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
M. Carter Cornwall
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

Single isolated photoreceptors can be taken through a visual cycle of light adaptation by bleaching visual pigment, followed by dark adaptation when supplied with 11–cis retinal. Light adaptation after bleaching is manifested by faster response kinetics and a permanent reduction in sensitivity to light flashes, presumed to be due to the presence of bleached visual pigment. The recovery of flash sensitivity during dark adaptation is assumed to be due to regeneration of visual pigment to pre-bleach levels. In previous work, the outer segments of bleached, light-adapted cells were exposed to 11–cis retinal. In the present work, the cell bodies of bleached photoreceptors were exposed. We report a marked difference between rods and cones. Bleached cones recover sensitivity when their cell bodies are exposed to 11–cis retinal. Bleached rods do not. These results imply that retinal can move freely along the cone photoreceptor, but retinal either is not taken up by the rod cell body or retinal cannot move from the rod cell body to the rod outer segment. The free transfer of retinal along cone but not along rod photoreceptors could explain why, during dark adaptation in the retina, cones have access to a store of 11–cis retinal which is not available to rods. Additional experiments investigated the movement of retinal along bleached rod outer segments. The results indicate that retinal can move along the rod outer segment, but that this movement is slow, occurring at about the same rate as the regeneration of visual pigment.

Keywords

Photoreceptors11-cis retinalRetinal movementVisual cycle
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 2 , March 1994 , pp. 389 - 399
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alpern, M., Maaseidvaag, F. & Ohba, N. (1971). The kinetics of cone visual pigments in man. Vision Research 11, 539–549.CrossRefGoogle ScholarPubMed
Bäckström, A.-C. & Hemilä, S.O. (1979). Dark-adaptation in frog rods: Changes in the stimulus response function. Journal of Physiology 287, 107–125.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589–611.CrossRefGoogle ScholarPubMed
Bonting, S.L., Rotmans, J.P. & Daemen, F.J.M. (1973). Chromophore migration after illumination of rhodopsin. In Biochemistry and Physiology of Visual Pigments, ed. Langer, H., pp. 39–44. Berlin: Springer-Verlag.CrossRefGoogle Scholar
BUNT-Milam, A.H. & Saari, J.C. (1983). Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. Journal of Cell Biology 97, 703–712.CrossRefGoogle ScholarPubMed
Chader, G.J. (1989). Interphotoreceptor retinoid-binding protein (IRBP). A model protein for molecular biological and clinically relevant studies. Investigative Ophthalmology and Visual Science 30, 7–30.Google Scholar
Coolen, A.C.C. & Van norren, D. (1988). Kinetics of human cone photopigments explained with a Rushton-Henry model. Biological Cybernetics 58, 123–128.CrossRefGoogle ScholarPubMed
Cornwall, M.C., Fein, A. & Macnichol, E.F., JR. (1983). Spatial localization of bleaching adaptation in isolated vertebrate rod photoreceptors. Proceedings of the National Academy of Sciences of the U. S. A. 80, 2785–2788.CrossRefGoogle ScholarPubMed
Cornwall, M.C., Fein, A. & Macnichol, E.F. Jr (1990). Cellular mechanisms that underlie bleaching and background adaptation. Journal of General Physiology 96, 345–372.CrossRefGoogle ScholarPubMed
Das, S.R., Bhardwaj, N., Kjeldbye, H. & Gouras, P. (1992). Muller cells of chicken retina synthesize 11-cis retinol. Biochemical Journal 285, 907–913.CrossRefGoogle ScholarPubMed
Das, S.R. & Gouras, P. (1993). Chicken photoreceptor outer segments oxidize 11-cis retinol. Investigative Ophthalmology and Visual Science (Suppl.) 34, 831.Google Scholar
Dowling, J.E. (1960). Chemistry of visual adaptation in the rat. Nature 168, 114–118.CrossRefGoogle Scholar
Edidin, M. (1974). Rotational and translational diffusion in membranes. Annual Review of Biophysics and Bioengineering 3, 179–201.CrossRefGoogle ScholarPubMed
Goldstein, E.B. (1967). Early receptor potential of the isolated frog (Rana pipiens) retina. Vision Research 7, 837–845.CrossRefGoogle ScholarPubMed
Goldstein, E.B. (1970). Cone pigment regeneration in the isolated frog retina. Vision Research 10, 1065–1068.CrossRefGoogle ScholarPubMed
Grabowski, S.R. & Pak, W.L. (1975). Intracellular recordings of rod responses during dark adaptation. Journal of Physiology 247, 363–391.CrossRefGoogle ScholarPubMed
Hodgkin, A.L., Mcnaughton, P.A., Nunn, B.J. & Yau, K.-W. (1984). Effect of ions on retinal rods from Bufo marinus. Journal of Physiology 350, 649–680.CrossRefGoogle ScholarPubMed
Hodgkin, A.L. & O≈bryan, P.M. (1977). Internal recording of the early receptor potential in turtle cones. Journal of Physiology 267, 737–766.CrossRefGoogle ScholarPubMed
Hollins, M. & Alpern, M. (1973). Dark adaptation and visual pigment regeneration in human cones. Journal of General Physiology 62, 430–447.CrossRefGoogle ScholarPubMed
Hood, D.C. & Hock, P.A. (1973). Recovery of cone receptor activity in the frog≈s isolated retina. Vision Research 13, 1943–1951.CrossRefGoogle ScholarPubMed
Hubbard, R., Brown, P.K. & Bownds, D. (1971). Methodology of vitamin A and visual pigments. Methods in Enzymology 18, 615–653.CrossRefGoogle Scholar
Jin, J., Jones, G.J. & Cornwall, M.C. (1991). The movement of retinal along cone and rod photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 32, 670.Google Scholar
Jones, G.J. (1974). Electron microscopy of frog rod outer segments after fixation with aldehydes. Journal of Cell Science 16, 199–219.CrossRefGoogle Scholar
Jones, G.J., Crouch, R.K., Wiggert, B., Cornwall, M.C. & Chader, G.J. (1989). Retinoid requirements for recovery of sensitivity after visual pigment bleaching in isolated photoreceptors. Proceedings of the National Academy of Sciences of the U. S. A. 86, 9606–9610.CrossRefGoogle ScholarPubMed
Jones, G.J., Fein, A., Macnichol, E.F. Jr & Cornwall, M.C. (1993). Visual pigment bleaching in isolated salamander retinal cones: Microspectrophotometry and light adaptation. Journal of General Physiology, 102, 483–502.CrossRefGoogle ScholarPubMed
Kaplan, M.W. (1984). Distribution and axial diffusion of retinol in bleached rod outer segments of frogs (Rana pipiens). Experimental Eye Research 40, 721–729.CrossRefGoogle Scholar
Kawaguchi, T., Hamanaka, T. & Kito, Y. (1986). Kinetic study of transfer of 11–cis-retinal between rod outer segment membranes using regeneration of rhodopsin. Biophysical Chemistry 24, 5–12.CrossRefGoogle ScholarPubMed
Leibovic, K.N., Dowling, J.E. & Kim, Y.Y. (1987). Background and bleaching equivalence in steady-state adaptation of vertebrate rods. Journal of Neuroscience 7, 1056–1063.CrossRefGoogle ScholarPubMed
Liebman, P.A. (1972). Microspectrophotometry of photoreceptors. In Handbook of Sensory Physiology, Vol. VII/1, Photochemistry of Vision, ed. Dartinall, H.J.A., pp. 481–528. Berlin: Springer-Verlag.Google Scholar
Makino, C.L., Howard, L.N. & Williams, T.P. (1990). Axial gradients of rhodopsin in light-exposed retinal rods of the toad. Journal of General Physiology 96, 1199–1220.CrossRefGoogle ScholarPubMed
Mangini, N.J & Pepperberg, D.R. (1988). Immunolocalization of 48K in rod photoreceptors. Investigative Ophthalmology and Visual Science 29, 1221–1234.Google ScholarPubMed
Normann, R.A. & Perlman, I. (1990). Background and bleaching adaptation in luminosity type horizontal cells in the isolated turtle retina. Journal of Physiology 421, 321–341.CrossRefGoogle ScholarPubMed
Perlman, J.I., Nodes, B.R. & Pepperberg, D.R. (1982). Utilization of retinoids in the bullfrog retina. Journal of General Physiology 80, 885–913.CrossRefGoogle ScholarPubMed
Rando, R.R. (1990). The chemistry of vitamin A and vision. Angewandte Chemie 29, 461–480.CrossRefGoogle Scholar
Roof, D.J. & Heuser, J.E. (1982). Surfaces of rod disc membranes: Integral membrane components. Journal of Cell Biology 95, 487–500.CrossRefGoogle Scholar
Rushton, W.A.H. (1961). Rhodopsin measurement and dark-adaptation in a subject deficient in cone vision. Journal of Physiology 156, 193–205.CrossRefGoogle Scholar
Rushton, W.A.H. (1972). Visual pigments in man. In Handbook of Sensory Physiology, Vol. VII/1, Photochemistry of Vision, ed. Dartnall, H.J.A., pp. 365–394. Berlin: Springer-Verlag.Google Scholar
Rushton, W.A.H. & Henry, G.H. (1968). Bleaching and regeneration of cone pigments in man. Vision Research 8, 617–631.CrossRefGoogle ScholarPubMed
Saari, J.C. (1990). Enzymes and proteins of the mammalian visual cycle. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 363–381. Oxford: Pergamon Press.Google Scholar
Schnapf, J.L. (1983). Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments. Journal of Physiology 343, 147–159.CrossRefGoogle ScholarPubMed
Sears, R.C. & Kaplan, M.W. (1989). Axial diffusion of retinol in isolated frog rod outer segments following substantial bleaches of visual pigment. Vision Research 29, 1485–1492.CrossRefGoogle ScholarPubMed
Szuts, E.Z. & Hárosi, F.I. (1991). Solubility of retinoids in water. Archives of Biochemistry and Biophysics 287, 297–304.CrossRefGoogle ScholarPubMed
Williams, T.P. & Penn, J.S. (1985). Intracellular topography of rho dopsin regeneration in vertebrate rods. Journal of General Physiology 86, 413–422.CrossRefGoogle Scholar
Yau, K.-W., Mcnaughton, P.A. & Hodgkin, A.L. (1981). Effect of ions on the light-sensitive current in retinal rods. Nature 292, 502–505.CrossRefGoogle ScholarPubMed
Yoshikami, S. & Nöll, G.N. (1978). Isolated retinas synthesize visual pigments from retinol congeners delivered by liposomes. Science 200, 1393–1395.CrossRefGoogle Scholar