Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T12:34:13.421Z Has data issue: false hasContentIssue false

Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light

Published online by Cambridge University Press:  02 June 2009

Adrian G. Palacios
Affiliation:
Department of Biology, Yale University, New Haven
Timothy H. Goldsmith
Affiliation:
Department of Biology, Yale University, New Haven
Gary D. Bernard
Affiliation:
Boeing Commercial Airplane Group, Seattle

Abstract

Photocurrents of cones in the retinas of a small fish, Danio aequipinnatus (Cyprinidae) were recorded with suction pipette electrodes. Spectral sensitivity was measured between 277 and 697 nm. Four spectral classes of cone were found, with λmax at 560, 480, 408, and 358 nm. For the latter, we provide the first complete characterization of spectral sensitivity of a vertebrate ultraviolet (UV) photoreceptor. All cones responded with similar kinetics, except for a subset of the 560-nm cones, which were distinctly faster. The a-bands of the three cones absorbing maximally in the visible have the same bandwidth when log sensitivity is plotted versus normalized frequency, and in this respect they are indistinguishable from primate cones (“Mansfield's rule’). An eighth-degree polynomial in λmax/λ based on this combined data set (fish, primate) is presented as a template that is likely to have predictive value in describing cone spectra from other vertebrates. The α−band of the UV cone, however, is somewhat narrower than predicted by this function, is similar to other UV visual pigments, and an eighth-degree polynomial that describes its shape is also presented. These measurements also provide information on the β−band (i.e. cis peak region), difficult to obtain by microspectrophotometry. The β−band of cone pigments is found at longer wavelengths as the α−band shifts toward the red. A secondary rise in cone sensitivity around 280 nm indicates that photons absorbed by aromatic amino acids in the opsin (γ−band) excite the transduction cascade, but the quantum efficiency is not as high as when absorption occurs in the retinal-protein chromophore.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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

Axelrod, H. R. & Schultz, L. P. (1990). Handbook of Tropical Aquarium Fishes. T.F.H. Publications, Neplune City, NJ.Google Scholar
Baylor, D. A. & Hodokin, A. L. (1973). Detection and resolution of visual stimuli by turtle photoreceptors. Journal of Physiology 234, 163198.CrossRefGoogle ScholarPubMed
Baylor, D. A., Hodgkin, A. L. & Lamb, T. D. (1974). The electrical response of turtle cones to flashes and steps of light. Journal of Physiology 242, 685727.CrossRefGoogle ScholarPubMed
Baylor, D. A., Lamb, T. D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589611.CrossRefGoogle ScholarPubMed
Baylor, D. A., Nunn, B. J. & Schnapf, J. L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaco fascicularis. Journal of Physiology 357, 575607.CrossRefGoogle Scholar
Baylor, D. A., Nunn, B. J. & Schnapf, J. L. (1987). Spectral sensitivity of cones of the monkey Macaco fascicularis. Journal of Physiology 390, 145160.CrossRefGoogle Scholar
Bernard, G. D. (1987). Spectral characterization of butterfly L-receptors using extended Dartnall/MacNichol template functions. Journal of the Optical Society of America A 4, 123.Google Scholar
Bowmaker, J. K. & Kunz, Y. W. (1987). Ultraviolet receptors, tetra-chromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): Age-dependent changes. Vision Research 27, 21012108.CrossRefGoogle Scholar
Bowmaker, J. K., Thorpe, A. & Douglas, R. H. (1991). Ultraviolet-sensitive cones in the goldfish. Vision Research 31, 349352.Google Scholar
Branchek, T. & Bremiller, R. (1984). The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure. Journal of Comparative Neurology 224, 107115.Google Scholar
Collins, F. D., Love, R. M. & Morton, R. A. (1952). Studies in rhodopsin. 4: Preparation of rhodopsin. Biochemical Journal 51, 292298.CrossRefGoogle ScholarPubMed
Creighton, T. E. (1984). Proteins: Structures and Molecular Properties. New York: W.H. Freeman and Company.Google Scholar
Dartnall, H. J. A. (1953). The interpretation of spectral sensitivity curves. British Medical Bulletin 9, 2430.CrossRefGoogle ScholarPubMed
Dartnall, H. J. A. (1972). Photosensitivity. In Handbook of Sensory Physiology, VII/1, Photochemistry of Vision, ed. Dartnall, H. J. A., pp. 122145. Berlin, Heidelberg, New York: Springer-Verlag.Google Scholar
Douglas, R. H. & Mcguigan, M. C. (1989). The spectral transmission of freshwater teleost ocular media – an interspecific comparison and a guide to potential ultraviolet sensitivity. Vision Research 29, 871879.CrossRefGoogle Scholar
Goldsmith, T. H. (1994). Ultraviolet receptors and color vision: Evolutionary implications and a dissonance of paradigms. Vision Research 34, 14791487.CrossRefGoogle Scholar
Hamdorf, K., Paulsen, R. & Schwemer, J. (1973). Photoregeneration and sensitivity control of photoreceptors of invertebrates. In Biochemistry and Physiology of Visual Pigments, ed. Langer, H., pp. 155166. Berlin, Heidelberg, New York: Springer-Verlag.Google Scholar
Hargrave, P. A., Mcdowell, J. H., Curtis, D. R., Wang, G. K., Juszczak, E., Fong, S.-L., Mohana Rao, J. K. & Argos, P. (1983). The structure of bovine rhodopsin. Biophysics of Structure and Mechanism 9, 235244.CrossRefGoogle ScholarPubMed
Hárosi, F. I. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 13591367.CrossRefGoogle ScholarPubMed
Hawryshyn, C. W. & Hárosi, F. I. (1994). Spectral characteristics of visual pigments in rainbow trout (Oncorhynchus mykiss). Vision Research 34, 13851392.Google Scholar
Johnson, R. L., Gran, K. B., Zankel, T. C., Boehm, M. F., Merbs, S. L., Nathans, J. & Nakanishi, K. (1993). Cloning and expression of goldfish opsin sequences. Biochemistry 32, 208214.CrossRefGoogle ScholarPubMed
Kropf, A. (1967). Intramolecular energy transfer in rhodopsin. Vision Research 7, 811818.CrossRefGoogle ScholarPubMed
Lamb, T. D., Mcnaughton, P. A. & YAU, K.-W.(1981). Spatial spread of activation and background desensitization in toad rod outer segments. Journal of Physiology 319, 463496.Google Scholar
Levine, J. S. & Macnichol, E. F. Jr. (1979). Visual pigments in teleost fishes: Effect of habitat, microhabitat and behavior on visual system evolution. Sensory Processes 3, 95131.Google ScholarPubMed
Lipetz, L. E. & Cronin, T. W. (1988). Application of an invariant spectral form to the visual pigments of crustaceans: Implications regarding the binding of the chromophore. Vision Research 28, 10831093.CrossRefGoogle Scholar
Loew, E. R. (1994). A third, ultraviolet-sensitive visual pigment in the Tokay gecko (Gekko gekko). Vision Research 34, 14271431.Google Scholar
Low, J. C., Yamada, M. & Djamgoz, M. B A. (1991). Voltage clamp study of electrophysiologically-identified horizontal cells in carp retina. Vision Research 31, 437449.CrossRefGoogle ScholarPubMed
Lythooe, J. N. (1979). The Ecology of Vision. Oxford: Clarendon Press.Google Scholar
Macnichol, E. F. Jr. (1986). A unifying presentation of photopigment spectra. Vision Research 26, 15431556.CrossRefGoogle ScholarPubMed
Maier, E. J. & Bowmaker, J. K. (1993). Colour vision in the passeri-form bird, Leiothrix lutea: Correlation of visual pigments, absorbance, and oil droplet transmission with spectral sensitivity. Journal of Comparative Physiology A 172, 295301.CrossRefGoogle Scholar
Makino, C. L., Taylor, W. R. & Baylor, D. A. (1991). Rapid charge movements and photosensitivity of visual pigments in salamander rods and cones. Journal of Physiology 442, 761780.CrossRefGoogle ScholarPubMed
Mansfield, R. J. W. (1985). Primate photopigments and cone mechanisms. In The Visual System, ed. Fein, A. & Levine, J. S., pp. 89106. New York: Alan R. Liss, Inc.Google Scholar
McFarland, W. N. & Loew, E. R. (1994). Ultraviolet visual pigments in marine fishes of the family Pomacentridae. Vision Research 34, 13931396.Google Scholar
Meyer, A., Biermann, C. H. & Orti, G. (1993). The phylogenetic position of the zebrafish (Danio rerio), a model system in developmental biology: An invitation to the comparative method. Proceedings of the Royal Society B (London) 252, 231236.Google Scholar
Miller, J. L. & Korenbrot, J. I. (1993). Phototransduction and adaptation in rods, single cones, and twin cones of the striped bass retina: A comparative study. Visual Neuroscience 10, 653667.CrossRefGoogle ScholarPubMed
Morton, R. A. (1972). The chemistry of visual pigments. In Handbook of Sensory Physiology, VII/I, Photochemistry of Vision, ed. Dart-Nall, H. J. A., pp. 3368. Berlin, Heidelberg, New York: Springer-Verlag.Google Scholar
Mote, M. I. & Wehner, R. (1980). Functional characteristics of photo-receptors in the compound eye and ocellus of the desert ant, Cataglyphis bicolor. Journal of Comparative Physiology 137, 6371.CrossRefGoogle Scholar
Naka, K. I. & Rushton, W. A. H. (1966). S-potentials from colour units in the retina of fish (Cyprinidae). Journal of Physiology 185, 536555.CrossRefGoogle ScholarPubMed
Nawrocki, L., Bremiller, R., Streisinger, G. & Kaplan, M. (1985). Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Research 25, 15691576.Google Scholar
Neumeyer, C. (1992). Tetrachromatic color vision in goldfish: Evidence from color mixture experiments. Journal of Comparative Physiology A 171, 639649.Google Scholar
Nunn, B. J., Schnapf, J. L. & Baylor, D. A. (1984). Spectral sensitivity of single cones in the retina of Macaco fasicularis. Nature 309, 264266.CrossRefGoogle Scholar
Palacios, A. G. & Goldsmith, T. H. (1993). Photocurrents in retinal rods of pigeons (Columba livia): Kinetics and spectral sensitivity. Journal of Physiology 471, 817829.CrossRefGoogle ScholarPubMed
Palacios, A. G., Srivastava, R. & Goldsmith, T. H. (1994). Spectral sensitivity of retinal cones in Danio malabaricus (giant danio). Society for Neuroscience Abstracts 20, 967.Google Scholar
Pande, C., Deng, H., Rath, P., Callender, R. H. & Schwemer, J. (1987). Resonance Raman spectroscopy of an ultraviolet-sensitive insect rhodopsin. Biochemistry 26, 74267430.CrossRefGoogle ScholarPubMed
Partridge, J. C. & Degrip, W. J. (1991). A new template for rhodopsin (vitamin A1 based) visual pigments. Vision Research 31, 619630.CrossRefGoogle ScholarPubMed
Pepe, I. M., Schwemer, J. & Paulsen, R. (1982). Characteristics of retinal-binding proteins from the honeybee retina. Vision Research 22, 775781.CrossRefGoogle ScholarPubMed
Perry, R. J. & Mcnaughton, P. A. (1991). Response properties of cones from retina of the tiger salamander. Journal of Physiology 433, 561587.CrossRefGoogle ScholarPubMed
Robinson, J., Schmitt, E. A., Hárosi, F. I., Reece, R. J. & Dowling, J. E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the U.S.A. 90, 60096012.CrossRefGoogle ScholarPubMed
Robinson, J. & Dowling, J. E. (1994). A vertebrate ultraviolet-sensitive visual pigment: Localization, structure, and spectral tuning. Sensornye Sistemy 8, 118126.Google Scholar
Schwemer, J., Pepe, I. M., Paulsen, R. & Cugnoli, C. (1984). Light induced trans-cis isomerization of retinal by a protein from honeybee retina. Journal of Comparative Physiology A 154, 549554.Google Scholar
Smith, W. C. & Goldsmith, T. H. (1991). The role of retinal photo-isomerase in the visual cycle of the honeybee. Journal of General Physiology 97, 143165.Google Scholar
Stavenga, D. A., Smits, R. P. & Hoenders, B. J. (1993). Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Research 33, 10111017.CrossRefGoogle ScholarPubMed
Teale, F. W. J. & Weber, G. (1957). Ultraviolet fluorescence of the aromatic amino acids. Biochemical Journal 65, 476482.Google Scholar
Uchida, K. & Morita, Y. (1990). Intracellular responses from UV-sensitive cells in the photosensory pineal organ. Brain Research 534, 237242.CrossRefGoogle ScholarPubMed
Wald, G., Brown, P. K. & Smith, P. H. (1955). lodopsin. Journal of General Physiology 38, 623681.CrossRefGoogle Scholar
Zeiger, J. & Goldsmith, T. H. (1993). Packaging of rhodopsin and porphyropsin in the compound eye of the crayfish. Visual Neuroscience 10, 193202.Google Scholar