Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T12:05:07.921Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification of retinal neurons in a regressive rodent eye (the naked mole-rat)

Published online by Cambridge University Press:  23 June 2004

STEPHEN L. MILLS  and
KENNETH C. CATANIA
STEPHEN L. MILLS
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston
KENNETH C. CATANIA
Affiliation:
Department of Biological Sciences, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

The retina consists of many parallel circuits designed to maximize the gathering of important information from the environment. Each of these circuits is comprised of a number of different cell types combined in modules that tile the retina. To a subterranean animal, vision is of relatively less importance. Knowledge of how circuits and their elements are altered in response to the subterranean environment is useful both in understanding processes of regressive evolution and in retinal processing itself. We examined common cell types in the retina of the naked mole-rat, Heterocephalus glaber with immunocytochemical markers and retrograde staining of ganglion cells from optic nerve injections. The stains used show that the naked mole-rat eye has retained multiple ganglion cell types, 1–2 types of horizontal cell, rod bipolar and multiple types of cone bipolar cells, and several types of common amacrine cells. However, no labeling was found with antibodies to the dopamine-synthesizing enzyme, tyrosine hydroxylase. Although most of the well-characterized mammalian cell types are present in the regressive mole-rat eye, their structural organization is considerably less regular than in more sighted mammals. We found less precision of depth of stratification in the inner plexiform layer and also less precision in their lateral coverage of the retina. The results suggest that image formation is not very important in these animals, but that circuits beyond those required for circadian entrainment remain in place.

Keywords

Mole-ratRegressive evolutionEyeVisionRetina
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 2 , March 2004 , pp. 107 - 117
Copyright
2004 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

Baldridge, W.H. & Ball, A.K. (1991). Background illumination reduces horizontal cell receptive-field size in both normal and 6-hydroxydopamine-lesioned goldfish retinas. Visual Neuroscience 7, 441–450.CrossRefGoogle Scholar
Bellesta, J., Terenghi, G., Thibault, J., & Polak, J.M. (1984). Putative dopamine-containing cells in the retina of seven species demonstrated by tyrosine hydroxylase immunocytochemistry. Neuroscience 12, 1147–1156.CrossRefGoogle Scholar
Berson, D.M., Dunn, F.A., & Takao, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070–1073.CrossRefGoogle Scholar
Boycott, B.B. & Wässle, H. (1999). Parallel processing in the mammalian retina: The Proctor lecture. Investigive Ophthalmology and Visual Science 40, 1313–1327.Google Scholar
Brecha, N.C., Oyster, C.W., & Takahashi, E.S. (1984). Identification and characterization of tyrosine hydroxylase immunoreactive amacrine cells. Investigative Ophthalmology and Visual Science 25, 66–70.Google Scholar
Bronchti, G., Rado, R., Terkel, J., & Wollberg, Z. (1991). Retinal projections in the blind mole rat: A WGA-HRP tracing study of a natural degeneration. Developmental Brain Research 58, 81–84.CrossRefGoogle Scholar
Casini, G., Rickman, D.W., & Brecha, N.C. (1995). AII amacrine cell population in the rabbit retina: identification by parvalbumin immunoreactivity. Journal of Comparative Neurology 356, 132–142.CrossRefGoogle Scholar
Catania, K.C. & Remple, M.S. (2002). Somatosensory cortex dominated by the representation of teeth in the naked mole rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 99, 5692–5697.CrossRefGoogle Scholar
Cernuda-Cernuda, R., DeGrip, W.J., Cooper, H.M., Nevo, E., & Garcia-Fernández, J.M. (2002). The retina of Spalax ehrenbergi: Novel histologic features supportive of a modified photosensory role. Investigative Ophthalmology and Visual Science 43, 2374–2383.Google Scholar
Cernuda-Cernuda, R., Garcia-Fernández, J.M., Gordign, M.C.M., Bovee-Guerts, P., & DeGrip, W.J. (2003). The eye of the african mole-rat Cryptomys anselli: To see or not to see? European Journal of Neuroscience 17, 709–720.Google Scholar
Cooper, H.M., Herbin, M., & Nevo, E. (1993a). Visual system of a naturally microphthalmic mammal: The blind mole rat, Spalax ehrenbergi. Journal of Comparative Neurology 328, 313–350.Google Scholar
Cooper, H.M., Herbin, M., & Nevo, E. (1993b). Ocular regression conceals adaptive progression of the visual system in a blind subterranean mammal. Nature 361, 156–159.Google Scholar
David-Gray, Z.K., Bellingham, J., Munoz, M., Avivi, A., Nevo, E., & Foster, R.G. (2002). Adaptive loss of ultraviolet-sensitive/violet-sensitive (UVS/VS) cone opsin in the blind mole rat (Spalax ehrenbergi). European Journal of Neuroscience 16, 1186–1194.CrossRefGoogle Scholar
Eckenstein, F. & Thoenen, H. (1982). Production of specific antisera and monoclonal antibodies to choline acetyltransferase: Characterization and use for identification of cholinergic neurons. EMBO Journal 1, 363–368.Google Scholar
Famiglietti, E.V. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138–144.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Grünert, U., Martin, P.R., & Wässle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 348, 607–627.CrossRefGoogle Scholar
Hamano, K., Kiyama, H., Emson, P.C., Manabe, R., Nakauchi, M., & Tohyama, M. (1990). Localization of two calcium-binding proteins, calbindin (28 kD) and parvalbumin (12 kD) in the vertebrate retina. Journal of Comparative Neurology 302, 417–424.CrossRefGoogle Scholar
Hannibal, J., Hindersson, P., Nevo, E., & Fahrenkrug, J. (2002). The circadian photopigment melanopsin is expressed in the blind subterranean mole rat, Spalax. Neuroreport 13, 1411–1414.CrossRefGoogle Scholar
Hattar, S., Liao, H.W., Takao, M., Berson, D.M., & Yau, K.W. (2002). Melanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science 295, 1065–1070.CrossRefGoogle Scholar
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. Journal of Comparative Neurology 424, 1–23.3.0.CO;2-V>CrossRefGoogle Scholar
Jeon, C.J., Strettoi, E., & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 8936–8946.CrossRefGoogle Scholar
Kolb, H., Linberg, K.A., & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.CrossRefGoogle Scholar
Marc, R.E. & Jones, B.W. (2002). Molecular phenotyping of retinal ganglion cells. Journal of Neuroscience 22, 413–427.CrossRefGoogle Scholar
Massey, S.C. & Mills, S.L. (1996). A calbindin-immunoreactive bipolar cell type in the rabbit retina. Journal of Comparative Neurology 366, 15–33.3.0.CO;2-N>CrossRefGoogle Scholar
Massey, S.C. & Mills, S.L. (1999). An antibody to calretinin stains AII amacrine cells in the rabbit retina: Double label and confocal analysis, Journal of Comparative Neurology 411, 3–18.Google Scholar
Mills, S.L. & Massey, S.C. (1994). Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina. Visual Neuroscience 11, 549–560.CrossRefGoogle Scholar
Mills, S.L. & Massey, S.C. (1999). AII amacrine cells limit scotopic acuity in central macaque retina: An analysis with calretinin labeling, confocal microscopy and intracellular dye injection. Journal of Comparative Neurology, 411, 19–34.3.0.CO;2-4>CrossRefGoogle Scholar
Negroni, J., Bennett, N.C., & Cooper, H. (2003). Organization of the circadian system in the subterranean mole rat, Crpytomys hottentotus (Bathyergidae). Brain Research 967, 48–62.CrossRefGoogle Scholar
Nevo, E. (1999). Mosaic evolution of subterranean mammals: regression, progression, and global convergence. Oxford, UK: Oxford University Press.
Panda, S., Provencio, I., Tu, D.C., Pires, S.S., Rollag, M.D., Castrucci, A.M., Pletcher, M.T., Sato, T.K., Wiltshire, T., Andahazy, M., Kay, S.A., Van Gelder, R.N., & Hogenesch, J.B. (2003). Melanopsin is required for non-image-forming photic responses in blind mice. Science 301, 525–527.CrossRefGoogle Scholar
Pasteels, B., Rogers, J., Blachier, F., & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.Google Scholar
Peichl, L. & Gonzalez-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig. Visual Neuroscience 11, 501–517.CrossRefGoogle Scholar
Peichl, L., Sandmann, D., & Boycott, B.B. (1998). Comparative anatomy and function of mammalian horizontal cells. In Development and Organization of the Retina, NATO ASI Series A, Vol. 299, ed. Chalupa, L. & Finlay, B., pp. 147–172. New York: Plenum Press.CrossRef
Peichl, L., Němec, P., & Burda, H. (2004). Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). European Journal of Neuroscience 19, 1545–1558.CrossRefGoogle Scholar
Reyes, A., Gissi, C., Catzeflis, F., Nevo, E., Pesole, G., & Saccone, C. (2004). Congruent mammalian trees from mitochondrial and nuclear genes using Bayesian methods. Molecular Biology and Evolution 21, 397–403.Google Scholar
Ribelayga, C. & Mangel, S.C. (2003). Absence of circadian clock regulation of horizontal cell gap junctional coupling reveals two dopamine systems in the goldfish retina. Journal of Comparative Neurology 467, 243–253.CrossRefGoogle Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P., & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. Journal of Neuroscience 22, 3831–3843.CrossRefGoogle Scholar
Röhrenbeck, J., Wässle, H., & Heizmann, C.W. (1987). Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neuroscience Letters 77, 255–260.CrossRefGoogle Scholar
Röhrenbeck, J., Wässle, H., & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. European Journal of Neuroscience 1, 407–420.CrossRefGoogle Scholar
Sanyal, S., Jansen, H.G., DeGrip, W.G., Nevo, E., & DeJong, W.W. (1990). The eye of the blind mole-rat, Spalax ehrenbergi. Rudiment with hidden function? Investigative Ophthalmology and Visual Science 31, 1398–1404.Google Scholar
Strettoi, E. & Masland, R.H. (1996). The number of unidentified amacrine cells in the mammalian retina. Proceedings of the National Academy of Sciences of the U.S.A. 93, 14906–14911.CrossRefGoogle Scholar
Veruki, M.L. & Wässle, H. (1996). Immunohistochemistry localization of dopamine D1 receptors in rat retina. European Journal of Neuroscience 8, 2286–2297.CrossRefGoogle Scholar
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of AII amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle Scholar
Wässle, H., Grünert, U., & Röhrenbeck, J. (1993). Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin. Journal of Comparative Neurology 332, 407–420.CrossRefGoogle Scholar
Wässle, H., Grünert, U., Chun, M.H., & Boycott, B.B. (1995). The rod pathway of the macaque monkey retina: Identification of AII-amacrine cells with antibodies against calretinin. Journal of Comparative Neurology 361, 537–551.CrossRefGoogle Scholar
Weiler, R., Baldridge, W.H., Mangel, S.C., & Dowling, J.E. (1997). Modulation of endogenous dopamine release in the fish retina by light and prolonged darkness. Visual Neuroscience 14, 351–356.CrossRefGoogle Scholar
Witkovsky, P. & Dearry, A. (1991). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247–292.CrossRefGoogle Scholar
Wong, R.O., Henry, G.H., & Medveczky, C.J. (1986). Bistratified amacrine cells in the retina of the tammar wallaby—Macropus eugenii. Experimental Brain Research 63, 102–105.Google Scholar