Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-24T20:52:37.651Z Has data issue: false hasContentIssue false

Photoreceptor distribution in the retina of adult Pacific salmon: Corner cones express blue opsin

Published online by Cambridge University Press:  26 June 2007

CHRISTIANA L. CHENG
Affiliation:
Department of Biological Sciences, Simon Fraser University, British Columbia, Canada
IÑIGO NOVALES FLAMARIQUE
Affiliation:
Department of Biological Sciences, Simon Fraser University, British Columbia, Canada

Abstract

The retina of salmonid fishes has two types of cone photoreceptors: single and double cones. At the nuclear level, these cones are distributed in a square mosaic such that the double cones form the sides of the square and the single cones occupy positions at the centre and at the corners of the square. Double cones consist of two members, one having visual pigment protein maximally sensitive to green light (RH2 opsin), the other maximally sensitive to red light (LWS opsin). Single cones can have opsins maximally sensitive to ultraviolet (UV) or blue light (SWS1 and SWS2 opsins, respectively). In Pacific salmonids, all single cones express UV opsin at hatching. Around the time of yolk sac absorption, single cones start switching opsin expression from UV to blue, in an event that proceeds from the ventral to the dorsal retina. This transformation is accompanied by a loss of single corner cones such that the large juvenile shows corner cones and UV opsin expression in the dorsal retina only. Previous research has shown that adult Pacific salmon have corner cones over large areas of retina suggesting that these cones may be regenerated and that they may express UV opsin. Here we used in-situ hybridization with cRNA probes and RT-PCR to show that: (1) all single cones in non-growth zone areas of the retina express blue opsin and (2) double cone opsin expression alternates around the square mosaic unit. Our results indicate that single cone driven UV sensitivity in adult salmon must emanate from stimulation of growth zone areas.

Type
Research Article
Copyright
© 2007 Cambridge University Press

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

REFERENCES

Ahlbert, I.-B. (1976). Organization of the cone cells in the retinas of salmon (Salmo salar) and trout (Salmo trutta trutta) in relation to their feeding habits. Acta Zoologica (Stockholm) 57, 1335.CrossRefGoogle Scholar
Ahlbert, I.-B. (1969). The organization of the cone cells in the retinae of four teleosts with different feeding habits (Perca fluvialis L., Lucioperca lucioperca L., Acerina cernua L., Coregonus albula L.). Arkiv für Zoologi 22, 445481.Google Scholar
Allison, W.T, Dann, S.G., Veldhoen, K.M. & Hawryshyn, C.W. (2006). Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. Journal of Comparative Neurology 499, 702715.CrossRefGoogle Scholar
Beaudet, L., Novales Flamarique, I. & Hawryshyn, C.W. (1997). Cone photoreceptor topography in the retina of sexually mature Pacific salmonid fishes. Journal of Comparative Neurology 383, 4959.3.0.CO;2-L>CrossRefGoogle Scholar
Bowmaker, J.K. & Kunz, Y.W. (1987). Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): Age-dependent changes. Vision Research 27, 21012108.CrossRefGoogle Scholar
Browman, H.I. & Hawryshyn, C.W. (1994). The developmental trajectory of ultraviolet photosensitivity in rainbow trout is altered by thyroxin. Vision Research 34, 13971406.CrossRefGoogle Scholar
Browman, H.I. & Hawryshyn, C.W. (1992). Thyroxine induces a precocial loss of ultraviolet photosensitivity in rainbow trout (Oncorhynchus mykiss, Teleostei). Vision Research 32, 23032312.CrossRefGoogle Scholar
Cheng, C.L. & Novales Flamarique, I. (2004). Opsin expression: New mechanism for modulating colour vision. Nature 428, 279.CrossRefGoogle Scholar
Cheng, C.L., Novales Flamarique, I., Hárosi, F.I., Rickers-Haunerland, J. & Haunerland N.H. (2006). Photoreceptor layer of salmonid fishes: Transformation and loss of single cones in juvenile fish. Journal of Comparative Neurology 495, 213235.CrossRefGoogle Scholar
Cheng, C.L., Gan, K. & Novales Flamarique, I. (2007). The ultraviolet opsin is the first opsin expressed during retinal development of salmonid fishes. Investigative Ophthalmology and Visual Science 48, 866873.CrossRefGoogle Scholar
Cook, J.E. & Chalupa, L.M. (2000). Retinal mosaics: New insights into an old concept. Trends in Neuroscience 23, 2634.CrossRefGoogle Scholar
Deutschlander, M.E., Greaves, D.K., Haimberger, T.J. & Hawryshyn, C.W. (2001). Functional mapping of ultraviolet photosensitivity during metamorphic transitions in a salmonid fish, Oncorhynchus mykiss. Journal of Experimental Biology 204, 24012413.Google Scholar
Engström, K. (1963). Cone types and cone arrangements in teleost retinae. Acta Zoologica (Stockholm) 44, 179243.CrossRefGoogle Scholar
Forsell, J., Ekström, P., Novales Flamarique, I., Holmqvist, B. (2001). Expression pattern of pineal UV- and green-like opsins in teleosts. Journal of Experimental Biology 204, 25172525.Google Scholar
Hawryshyn, C.W., Martens, G., Allison, T.W. & Anholt, B. (2003). Regeneration of ultraviolet-sensitive cones in the retinal cone mosaic of thyroxin-challenged post-juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206, 26652673.CrossRefGoogle Scholar
Hawryshyn, C.W., Arnold, M.G., Chiasson, D. & Martin, P.C. (1989). The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gardneri). Visual Neuroscience 2, 247254.CrossRefGoogle Scholar
Hoar, W.S. (1988). The physiology of smolting salmonids. In Fish Physiology, ed. Hoar, W.S. & Randall, D.J., pp. 275343. New York: Academic Press, Inc.CrossRef
Kunz, Y.W., Wildenburg, G., Goodrich, L. & Callaghan, E. (1994). The fate of ultraviolet receptors in the retina of the Atlantic salmon (Salmo salar). Vision Research 34, 13751383.CrossRefGoogle Scholar
Lyall, A.H. (1957a). Cone arrangements in teleost retinae. Quarterly Journal of Microscopy Science 98, 189201.Google Scholar
Lyall, A.H. (1957b). The growth of the trout retina. Quarterly Journal of Microscopy Science 98, 101110.Google Scholar
Martens, G.D. (2000). Topographical changes to the cone photoreceptor mosaic in thyroxin challenged rainbow trout (Oncorhynchus mykiss). University of Victoria Master Thesis, 134 pp.
Novales Flamarique, I. (2005). Temporal shifts in visual pigment absorbance in the retina of Pacific salmon. Journal of Comparative Physiology A 191, 3749.CrossRefGoogle Scholar
Novales Flamarique, I. (2002). Partial re-incorporation of corner cones in the retina of the Atlantic salmon (Salmo salar). Vision Research 42, 27372745.CrossRefGoogle Scholar
Novales Flamarique, I. (2001). Gradual and partial loss of corner cone-occupied area in the retina of rainbow trout. Vision Research 41, 30733082.CrossRefGoogle Scholar
Novales Flamarique, I. (2000). The ontogeny of ultraviolet sensitivity, cone disappearance and regeneration in the sockeye salmon Oncorhynchus nerka. Journal of Experimental Biology 203, 11611172.Google Scholar
Novales Flamarique, I. & Hawryshyn, C.W. (1996). Retinal development and visual sensitivity of young Pacific sockeye salmon (Oncorhynchus nerka). Journal of Experimental Biology 199, 869882.Google Scholar
Sower, S.A. & Schreck, C.B. (1982). Steroid and thyroid hormones during sexual maturation of coho salmon (Oncorhynchus kisutch) in seawater or freshwater. General Comparative Endocrinology 47, 4253.CrossRefGoogle Scholar
Veldhoen, K., Allison, T.W., Veldhoen, N., Anholt, B.R., Helbing, C.C. & Hawryshyn, C.W. (2006). Spatio-temporal characterization of retinal opsin gene expression during thyroid hormone-induced and natural development of rainbow trout. Visual Neuroscience 23, 169179.CrossRefGoogle Scholar
Youngson, A.F. & Webb, J.H. (1993). Thyroid hormone levels in Atlantic salmon (Salmo salar) during the return migration from the ocean to spawn. Journal of Fish Biology 42, 293300.CrossRefGoogle Scholar