Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T08:32:19.212Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunocytochemical localization of dopamine D1 receptors in the retina of mammals

Published online by Cambridge University Press:  02 June 2009

J. Nguyen-Legros ,
A. Simon ,
I. Caillé  and
B. Bloch
J. Nguyen-Legros
Affiliation:
INSERM U-86, Laboratoire de NeuroCytologie Oculaire, Paris Cedex, France
A. Simon
Affiliation:
INSERM U-86, Laboratoire de NeuroCytologie Oculaire, Paris Cedex, France
I. Caillé
Affiliation:
EP CNRS 74, Laboratoire d'histologie-Embryologie (UFR II), Université de Bordeaux II, Bordeaux Cedex, France
B. Bloch
Affiliation:
EP CNRS 74, Laboratoire d'histologie-Embryologie (UFR II), Université de Bordeaux II, Bordeaux Cedex, France
Get access Rights & Permissions [Opens in a new window]

Abstract

Dopamine is one of the major neurotransmitters in the retina. It is released from amacrine and interplexiform cells into both inner (IPL) and outer (OPL) plexiform layers. Several dopaminergic actions are known to occur through D1 receptors (D1R) but the precise location of these receptors has not been established. An antibody that recognizes the intracytoplasmic C-terminal of the rat D1R was used to detect D1R, immunohistochemically, in rats (Wistar and RCS), mouse, hamster, and macaque monkey retinas. The OPL was heavily stained in each species, consistent with the known actions of dopamine on horizontal cells. Three to five bands were observed in the IPL, depending on species. Three were in the a sublayer, the outermost of which was close to the amacrine cell layer, and may represent the massive dopamine input to the AII rod-amacrine cells. As observed in mice, where bipolar cells are D1-immunoreactive, the band located in sublayer 3 of the IPL may contain cone-bipolar cell terminals. A band of D1R-immunoreactivity in the b sublayer of the IPL contains ON-bipolar cell terminals and a second site of interaction between dopaminergic cells and the AII amacrine cells. This sublayer was absent from the RCS rat retina, suggesting a severe impairment of the rod-driven pathway following rod degeneration in these mutant rats. Cells in the ganglion cell layer exhibited relatively heavy staining, and may be ganglion cells or displaced amacrine cells. Some extrasynaptic localizations of D1R in the retina are suggested.

Keywords

SynapsePrimate foveaRCS ratsBipolar cells
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 545 - 551
Copyright
Copyright © Cambridge University Press 1997

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

Behrens, U.D. & Wagner, H-J. (1995). Localization of dopamine D-l receptors in vertebrate retinae. Neurochemistry International 27, 497–507.Google Scholar
Caillé, I., Dumartin, B., Le Moine, C., Begueret, J. & Bloch, B. (1995). Ontogeny of the D1, dopamine receptor in the rat striatonigral system: An immunohistochemical study. European Journal of Neuroscience 7, 714–722.CrossRefGoogle ScholarPubMed
Caillé, I., Dumartin, B. & Bloch, B. (1996). Ultrastructural localization of D1 dopamine receptor immunoreactivity in rat striatonigral neurons and its relation with dopaminergic innervation. Brain Research (in press).CrossRefGoogle ScholarPubMed
Cohen, A.I., O'Malley, K. & Meador-Woodruff, J. (1992). Mouse photoreceptors contain D4 receptors coupled to adenylate cyclase. Investigative Ophthalmology and Visual Science 33, 1404.Google Scholar
Dearry, A., Falardeau, P., Shores, C. & Caron, M.G. (1991). D2 dopamine receptors in the human retina. Cloning of cDNA and localization of messenger RNA. Cellular and Molecular Neurobiology 11, 437–454.CrossRefGoogle Scholar
Denis, P., Elena, P-P., Nordmann, J-P., Saraux, H. & Lapalus, P. (1990). Autoradiographic localization of D1 and D2 dopamine binding sites in the human retina. Neuroscience Letters 116, 81–86.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A. & Wagner, H-J. (1992). Localization and function of dopamine in the adult vertebrate retina. Neurochemistry International 20, 139–191.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ehinger, B. (1975). Synaptic organization of aminecontaining interplexiform cells of the goldfish and Cebus monkey retinas. Science 188, 270–273.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ehinger, B. (1978). Synaptic organization of the dopaminergic neurons in the rabbit retina. Journal of Comparative Neurology 180, 203–220.CrossRefGoogle ScholarPubMed
Elena, P.-P., Denis, P., Kosina-Boiz, M. & Lapalus, P. (1989). Dopamine receptors in rabbit and rat eye: Characterization and localization of DA1 and DA2 binding sites. Current Eye Research 8, 75–83.CrossRefGoogle ScholarPubMed
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461–478.CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E., Laties, A.M., Lam, D.M.K. & Hollyfield, J.G. (1982). Dopaminergic neurons in the human retina. Journal of Comparative Neurology 210, 65–79.CrossRefGoogle ScholarPubMed
Guenther, I., Witsch, V. & Zrenner, E. (1994). Inhibitory action of haloperidol, spiperone and SCH-23390 on calcium currents in rat retinal ganglion cells. Neuroreport 5, 1373–1376.Google Scholar
Hampson, E.C.G.M., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.CrossRefGoogle ScholarPubMed
Hampson, E.C.G.M., Weiler, R. & Vaney, D.I. (1994). pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina. Proceedings of the Royal Society B (London) 255, 67–72.Google ScholarPubMed
Hedden, W.L. & Dowling, J.E. (1978). The interplexiform cell system. II. Effects of dopamine on goldfish retinal neurons. Proceedings of the Royal Society B (London) 201, 27–55.Google Scholar
Heidelberger, R. & Matthews, G. (1994). Dopamine enhances CA2+ responses in synaptic terminals of retinal bipolar neurons. Neuroreport 5, 729–732.CrossRefGoogle ScholarPubMed
Hensler, J.G. & Dubocovich, M.I. (1988). GABAergic modulation of D1 dopamine receptor-mediated [3H]-acetylcholine release from rabbit retina. Archives of Pharmacology 337, 661–668.CrossRefGoogle ScholarPubMed
Hokoç, J.N. & Mariani, A.P. (1988). Synapses from bipolar cells onto dopaminergic amacrine cells in cat and rabbit retinas. Brain Research 461, 17–26.CrossRefGoogle Scholar
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–439.CrossRefGoogle ScholarPubMed
Kolb, H., Cuenca, N., Wang, H-H. & Dekorver, L. (1990). The synaptic organization of the dopaminergic amacrine cell in the cat retina. Journal of Neurocytology 19, 343–366.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Krizaj, D. & Witkovsky, P. (1993). Effects of submicromolar concentration of dopamine on photoreceptor to horizontal cell communication. Brain Research 627, 122–128.CrossRefGoogle ScholarPubMed
Liman, E.R., Knapp, A.G. & Dowling, J.E. (1989). Enhancement of kainate-gated currents in retinal horizontal cells by cyclic AMP-dependent protein kinase. Brain Research 481, 399–402.CrossRefGoogle ScholarPubMed
Liu, Y. & Lasater, E.M. (1994). Calcium currents in turtle retinal ganglion cells. 2. Dopamine modulation via a cyclic AMP-dependent mechanism. Journal of Neurophysiology 72, 730–741.Google Scholar
Maguire, G. & Werblin, F. (1994). Dopamine enhances a glutamategated ionic cuttent in OFF bipolar cells of the tiger salamander retina. Journal of Neuroscience 14, 6094–6101.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Hokoç, J.N. (1991). Synaptic organization of type-2 catecholamine amacrine cells in the rhesus monkey. Journal of Neurocytology 20, 332–342.CrossRefGoogle ScholarPubMed
Merchenthaler, I., Stankovics, J. & Gallyas, F. (1989). A highly sensitive one-step method for silver intensification of the nickel diaminobenzidine end product of peroxidase reaction. Journal of Histochemistry and Cytochemistry 37, 1563–1565.CrossRefGoogle Scholar
Morgan, I.G., Boelen, M.K. & Miethke, P. (1995). Pineal activity is under the control of retinal D1-dopaminergic pathways. NeuroReport 6, 446–448.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1990). The dopamine system of the teleost fish retina. Progress in Retinal Research 9, 1–48.CrossRefGoogle Scholar
Nguyen-Legros, J. (1988). Morphology and distribution of catecholamine neurons in mammalian retina. Progress in Retinal Research 7, 113–147.CrossRefGoogle Scholar
Nguyen-Legros, J., Krieger, M. & Simon, A. (1994). Immunohistochemical localization of L-DOPA and aromatic L-amino acid decarboxylase in the rat retina. Investigative Ophthalmology and Visual Science 35, 2906–2915.Google ScholarPubMed
Nguyen-Legros, J., Martin-Martinelli, E., Simon, A., Denoroy, L. & Vigny, A. (1986). Co-localization of tyrosine hydroxylase and phenylethanolamine N-methyltransferase immunoreactivity in the rat retina: A re-examination using double labelling on semi-thin sections. Experimental Eye Research 43, 575–584.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J., Moussafi, F. & Simon, A. (1990). Sclerally directed processes of dopaminergic interplexiform cells reach the outer nuclear layer in rat and monkey retina. Visual Neuroscience 4, 547–553.CrossRefGoogle ScholarPubMed
Perry, H.V. (1982). The ganglion cell layer of the mammalian retina. Progress in Retinal Research 1, 53–80.CrossRefGoogle Scholar
Piccolino, M., De Montis, G., Witkovsky, P., Strettoi, E., Cappagli, G., Porceddu, C., De Montis, M.G., Pepitoni, S., Biggio, G., Meller, E. & Bohmaker, K. (1989). Involvement of D1 and D2 dopamine receptors in the control of horizontal cell electrical coupling in the turtle retina. European Journal of Neuroscience 1, 247–256.CrossRefGoogle ScholarPubMed
Pourcho, R.G. (1982). Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101–109.CrossRefGoogle ScholarPubMed
Reichenbach, A. & Eberhardt, W. (1988). Cytotopographical specialization of enzymatically isolated rabbit Müller (glial), cells: K+ conductivity of the cell membrane. Glia 1, 191–197.CrossRefGoogle ScholarPubMed
Savy, C., Moussafi, F., Durand, J., Yelnik, J., Simon, A. & Nguyen-Legros, J. (1995). Distribution and spatial geometry of dopamine interplexiform cells in the retina. II. External arborizations in the adult rat and monkey. Journal of Comparative Neurology 355, 392–404.CrossRefGoogle Scholar
Schorderet, M. & Nowak, J.Z. (1990). Retinal dopamine D1 and D2 receptors: Characterization by binding and pharmacological studies and physiological functions. Cellular and Molecular Neurobiology 10, 303–305.CrossRefGoogle ScholarPubMed
Schwartz, E.A. (1993). L-glutamate conditionally modulates the K+ current of Müller glial cells. Neuron 10, 1141–1149.CrossRefGoogle Scholar
Simon, A., Caillé, I., Bloch, B. & Nguyen-Legros, J. (1995). Immunocytochemical localization of Dl dopamine receptors in the mammalian retina. Investigative Ophthalmology and Visual Science 36, S289.Google Scholar
Smiley, J.F., Levey, A.I., Ciliax, B.J. & Goldman-Rakic, P.S. (1994). D1dopamine receptor immunoreactivity in human and monkey cerebral cortex: Predominant extrasynaptic localization in dendritic spines. Proceedings of the National Academy of Sciences of the U.S.A. 91, 5720–5724.CrossRefGoogle Scholar
Stoof, J.C. (1989). Localization and pharmacology of some DA receptor complexes in the striatum and pituitary gland: Synaptic and non-synaptic communication. Acta Morphologica Neerl.-Scand 26, 115–130.Google Scholar
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 1271–1280.CrossRefGoogle ScholarPubMed
Törk, I. & Stone, J. (1979). Morphology of.catecholamine-containing amacrine cells in the cat's retina as seen in retinal whole mounts. Brain Research 169, 261–273.CrossRefGoogle ScholarPubMed
Tran, V.T. & Dickman, M. (1992). Differential localization of dopamine D1 and D2 receptors in rat retina. Investigative Ophthalmology and Visual Science 33, 1620–1626.Google ScholarPubMed
Van Haesendonck, E., Marc, R.E. & Missotten, L. (1993). New aspects of dopaminergic interplexiform cell organization in the goldfish retina. Journal of Comparative Neurology 333, 503–518.CrossRefGoogle ScholarPubMed
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of AII amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle Scholar
Vuvan, T., Geffard, M., Denis, P., Simon, A. & Nguyen-Legros, J. (1993). Radioimmunoligand characterization and immunohistochemical localization of dopamine D2 receptor on rods in the rat retina. Brain Research 614, 57–64.CrossRefGoogle ScholarPubMed
Wagner, H-J., Luo, B.G., Ariano, M.A., Sibley, D.R. & Stell, W.K. (1993). Localization of D2 dopamine receptors in vertebrate retinae with anti-peptide antibodies. Journal of Comparative Neurology 331, 469–481.CrossRefGoogle ScholarPubMed
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Review 71, 447–480.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Dearry, A. (1991). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247–292.CrossRefGoogle Scholar
Witkovsky, P., Nicholson, C., Rice, M.E., Bohmaker, K. & Meller, E. (1993). Extracellular dopamine concentration in the retina of the clawed frog Xenopus laevis. Proceedings of the National Academy of Sciences of the U.S.A. 90, 5667–5690.CrossRefGoogle ScholarPubMed
Yamada, M. & Saito, T. (1988). Effects of dopamine on bipolar cells in the carp retina. Biomedical Research 9, 125–130.Google Scholar
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopaminergic interplexiform cells in the goldfish retina. Visual Neuroscience 1, 13–19.CrossRefGoogle ScholarPubMed
Yeh, H.H., Batelle, B.A. & Puro, D.G. (1984). Dopamine regulates synaptic transmission mediated by cholinergic neurons of the rat retina. Neuroscience 13, 901–910.CrossRefGoogle ScholarPubMed
Zarbin, M.A., Wamsley, J.K., Palacios, J.M. & Kuhar, M.J. (1986). Autoradiographic localization of high affinity GABA, benzodiazepine, dopaminergic, adrenergic and muscarinic cholinergic receptors in the rat, monkey and human retina. Brain Research 374, 75–92.CrossRefGoogle ScholarPubMed