Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T12:40:23.479Z Has data issue: false hasContentIssue false
  • English
  • Français

Regional topography of rod and immunocytochemically characterized “blue” and “green” cone photoreceptors in rabbit retina

Published online by Cambridge University Press:  02 June 2009

E. V. Famiglietti  and
S. J. Sharpe
E. V. Famiglietti
Affiliation:
Department of Anatomy and Lions Sight Centre, University of Calgary, Calgary, Alberta, Canada T2N 4N1
S. J. Sharpe
Affiliation:
Department of Anatomy and Lions Sight Centre, University of Calgary, Calgary, Alberta, Canada T2N 4N1
Get access Rights & Permissions [Opens in a new window]

Abstract

Evidence from several sources indicates that the photoreceptors of rabbit retina include rods, green cones and blue cones, and that blue-green color opponency occurs in select retinal ganglion cells. One of us (Famiglietti) has identified wide-field cone bipolar cells as probable blue-cone-selective bipolars, and type C horizontal cells as possibly connected to blue cones. We wished to extend the analysis of blue cone pathways in rabbit retina and to characterize the topographic distribution of blue and green cones. Two monoclonal antibodies raised against chicken visual pigments are reported to label medium- and long-wavelength cones (COS-1) and short-wavelength cones (OS-2) in all mammalian retinas studied thus far (Szél and colleagues). Using selective labeling with these two antibodies and a nonselective method in nasal and temporal halves of the same retinas, we have found that densities of photoreceptors vary systematically, depending upon the size of the eye and age of the animal. In ‘standard’ New Zealand rabbits of 2–3 kg (2–3 months old), rods reached a peak density of about 300,000/mm2 just dorsal to the visual streak, while cones exhibit peak density at mid-visual streak of about 18,000/mm2. Published measurements of visual acuity in rabbit are less than predicted by this calculation. The ratio of cones to rods is significantly higher in ventral retina, where the density of cones declines to a plateau of 10,000–12,000/mm2, when compared to dorsal retina, where cones are uniformly distributed at a density of about 7000/mm2. The density of OS-2 labeled (presumably “blue”) cones is uniformly low, 1000–1500/mm2, in a wide expanse that includes dorsal retina, the visual streak, and much of ventral retina, except for a region of higher density along the vertical midline. We confirm that there is a far ventral horizontal region near the perimeter that is populated exclusively by a high density (about 13,000/mm2) of OS-2-positive cones (Juliusson and colleagues). This region does not extend to the ventral retinal margin, however, where cone density drops precipitously. Transitional zones between COS-1 and OS-2 labeling, in a region of relatively high and uniform cone density, where sums of COS-1 and OS-2 labeling are higher than expected and in which weakly and strongly labeled cones are intermixed, raise questions about the identities of the visual pigment epitopes, the possibility of double labeling, and therefore the possibility of dual expression of pigments in single cones. The “inverted- T -shaped” topography of higher density OS-2 labeling raises doubts about the significance of a ventral concentration of blue cones for visual function in rabbit retina.

Keywords

Blue conesGreen conesCone opsinColor visionRetinal developmentRetinal expansionVisual acuityBlue cone bipolar cells
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 6 , November 1995 , pp. 1151 - 1175
Copyright
Copyright © Cambridge University Press 1995

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

Boycott, B.B. & Hopkins, J.M. (1991). Cone bipolar cells and cone synapses in the primate retina. Visual Neuroscience 7, 49–60.CrossRefGoogle ScholarPubMed
Calderone, J.B. & Jacobs, G.H. (1994). Regional variations in sensitivity to UV light in the mouse retina. Investigative Ophthalmology 35, 2046.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. Journal of Physiology (London) 276, 257–276.CrossRefGoogle ScholarPubMed
Chiu, I.M. & Nathans, J. (1994). Blue cones and cone bipolar cells share transcriptional specificity as determined by expression of human blue visual pigment-derived transgenes. Journal of Neuroscience 14, 3426–3436.CrossRefGoogle ScholarPubMed
Cleland, B.G., Levick, W.R. & Sanderson, K.J. (1973). Properties of sustained and transient ganglion cells in the cat retina. Journal of Physiology (London) 228, 649–680.CrossRefGoogle ScholarPubMed
DeMonasterio, F.M. (1978). Spectral interactions in horizontal and ganglion cells of the isolated and arterially-perfused rabbit retina. Brain Research 150, 239–258.CrossRefGoogle Scholar
DeMonasterio, F.M., Schein, S.J. & McCrane, E.P. (1981). Staining of blue-sensitive cones of the macaque retina by a fluorescent dye. Science 213, 1278–1281.CrossRefGoogle ScholarPubMed
Enroth, Cugell C & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517–552.CrossRefGoogle Scholar
Famiglietti, E.V. (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1990). A new type of wide-field horizontal cell, presumably linked to blue cones, in rabbit retina. Brain Research 535, 174–179.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Sharpe, S.J. (1994). Differential topography of immunocytochemically labelled cones in rabbit retina. Investigative Ophthalmology and Visual Science 35, 2122.Google Scholar
Hill, R.M. (1962). Unit responses of the rabbit lateral geniculate nucleus to monochromatic light on the retina. Science 135, 98–99.CrossRefGoogle ScholarPubMed
Höllander, H. & Stone, J. (1972). Receptor pedicle density in the cat≈s retina. Brain Research 42, 497–502.CrossRefGoogle ScholarPubMed
Hughes, A. (1971). Topographic relationships between the anatomy and physiology of the rabbit visual system. Documenta Ophthalmologica 30, 33–159.CrossRefGoogle ScholarPubMed
Hughes, A. (1972). A schematic eye for the rabbit. Vision Research 12, 123–138.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Neitz, J. & Deegan, J.F., III (1991). Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353, 655–656.CrossRefGoogle ScholarPubMed
Jacobson, S.G., Franklin, K.B.J. & McDonald, W.I. (1976). Visual acuity of the cat. Vision Research 16, 1141–1143.CrossRefGoogle ScholarPubMed
Juliusson, B., Szél, A., Bergström, A., Ehinger, B. & van Veen, T. (1993). Reversed ratio of color specific cones in rabbit retinal transplants. Investigative Ophthalmology and Visual Science 34, 1096.Google Scholar
Juliusson, B., Bergström, A., Röhlich, P., Ehinger, B., van Veen, T. & Szél, A. (1994). Complementary cone fields of the rabbit retina. Investigative Ophthalmology and Visual Science 35, 811–818.Google ScholarPubMed
Klug, K., Tiv, N., Tsukamoto, Y., Sterling, P. & Schein, S.J. (1992). Blue cones contact off-midget bipolar cells. Society for Neuroscience Abstracts 18, 838.Google Scholar
Kouyama, N. & Marshak, D.W. (1992). Bipolar cells specific for blue cones in the macaque retina. Journal of Neuroscience 12, 1233–1252.CrossRefGoogle ScholarPubMed
Lerea, C.L., Bunt-Milam, A.H. & Hurley, J.B. (1989). Alpha-transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina. Neuron 3, 367–376.CrossRefGoogle ScholarPubMed
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit≈s retina. Journal of Physiology (London) 188, 285–307.CrossRefGoogle ScholarPubMed
Marc, R.E. & Sperling, H.G. (1977). Chromatic organization of primate cones. Science 196, 454–456.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984). Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature 308, 184–186.CrossRefGoogle ScholarPubMed
Nuboer, J.F.W. (1971). Spectral discrimination in a rabbit. Documenta Ophthalmologica 30, 279–298.CrossRefGoogle ScholarPubMed
Oyster, C.W., Takahashi, E.S. & Hurst, D.C. (1981). Density, soma size, and regional distribution of rabbit retinal ganglion cells. Journal of Neuroscience 1, 1331–1346.CrossRefGoogle ScholarPubMed
Provis, J.M. (1979). The distribution and size of ganglion cells in the retina of the pigmented rabbit: A quantitative analysis. Journal of Comparative Neurology 185, 121–138.CrossRefGoogle ScholarPubMed
Robinson, S.R., Dreher, B. & McCall, M.J. (1989). Nonuniform retinal expansion during the formation of the rabbit≈s visual streak: Implications for the ontogeny of mammalian retinal topography. Visual Neuroscience 2, 201–219.CrossRefGoogle ScholarPubMed
Rölich, P., van Veen, Th, & Szél, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166.CrossRefGoogle Scholar
Steinberg, R.H., Reid, M. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229–248.CrossRefGoogle ScholarPubMed
Szél, A., Diamantstein, T. & Röhlich, P. (1988). Identification of blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. Journal of Comparative Neurology 273, 593–602.CrossRefGoogle ScholarPubMed
Szél, A., Röhlich, P., Caffé, A.R., Juliusson, B., Aguirre, G. & van Veen, T. (1992). Unique topographic separation of two spectral classes of cones in the mouse retina. Journal of Comparative Neurology 325, 327–342.CrossRefGoogle ScholarPubMed
Szél, A., van Veen, T. & Röhlich, P. (1994). Retinal cone differentiation. Nature 370, 336.CrossRefGoogle ScholarPubMed
Vaney, D.I., Levick, W.R. & Thibos, L.N. (1981). Rabbit retinal ganglion cells. Receptive field classification and axonal conduction properties. Experimental Brain Research 44, 27–33.Google ScholarPubMed
van Hof, M.W. (1967). Visual acuity in the rabbit. Vision Research 7, 749–751.CrossRefGoogle ScholarPubMed
Walls, G.H. (1942). The Vertebrate Eye and Its Adaptive Radiation. Michigan: Cranbrook Press.Google Scholar
Wässle, H. (1971). Optical quality of the cat eye. Vision Research 11, 995–1006.CrossRefGoogle ScholarPubMed
Westheimer, G. (1962). Line-spread function of living cat eye. Journal of the Optical Society of America 52, 1326.Google Scholar
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. Journal of Comparative Neurology 310, 139–153.CrossRefGoogle ScholarPubMed