Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-25T21:15:56.685Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatial geometry of the dopamine innervation in the avascular area of the human fovea

Published online by Cambridge University Press:  02 June 2009

Claudine Savy ,
Axelle Simon  and
Jeanine Nguyen-Legros
Claudine Savy
Affiliation:
Laboratoire de Neurocytologie Oculaire (INSERM U-86), 15, rue de l' Ecole de Médecine, 75270, Paris06, France
Axelle Simon
Affiliation:
Laboratoire de Neurocytologie Oculaire (INSERM U-86), 15, rue de l' Ecole de Médecine, 75270, Paris06, France
Jeanine Nguyen-Legros
Affiliation:
Laboratoire de Neurocytologie Oculaire (INSERM U-86), 15, rue de l' Ecole de Médecine, 75270, Paris06, France
Get access Rights & Permissions [Opens in a new window]

Abstract

The dopamine (DA) innervation, labeled by tyrosine hydroxylase immunohistochemistry in a wholemounted human retina, is described in the avascular area of the fovea. Eleven DA neurons give rise to this innervation, among which five are interplexiform cells, so that the DA innervation consists of two plexuses: one is internal and is formed by the dendrites of all of the DA cells, and the other is external and is formed by the scleral processes of the interplexiform cells. Five concentric zones are delineated according to the focal plane in which the internal DA plexus is observed. The central zone 1 contains DA processes crossing in all directions. Zones 2 and 3 do not contain any cell bodies. In zone 3 the internal plexus begins to undergo a concentric arrangement, which is clearly observed in zones 4 and 5. The external DA innervation displays a different appearance in zones 1, 2, and 3, in which it consists of vertically oriented thin processes and terminals penetrating the outer nuclear layer, vs. zones 4 and 5 in which it consists of both the same type and horizontal processes lying in the outer plexiform layer. On the basis of DA-innervation appearance and distribution of labeled and unlabeled cell somata, it was concluded that zones 1, 2, and 3 contained the DA innervation of the foveola. DA processes filtering between photoreceptor cells are particularly well-observed in this region. This anatomical study of the DA innervation in the human fovea leads to a better understanding of the important role of DA in primate central vision and can be used as a reference for an approach of macular pathology.

Keywords

RetinaDopamineHumanFoveaTopology
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 5 , November 1991 , pp. 487 - 498
Copyright
Copyright © Cambridge University Press 1991

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

Ahnelt, P.K. & Pflug, R. (1986). Telodendrial contacts between foveolar-cone pedicles in the human retina. Experientia 42, 298–300.CrossRefGoogle ScholarPubMed
Ballantyne, A.J. & Michaelson, I.C. (1970). Textbook of the Fundus of the Eye. London: Livingstone, E. and S.Google Scholar
Bird, A.C. & Weale, R.A. (1974). On the retinal vasculature of the human fovea. Experimental Eye Research 19, 409–417.CrossRefGoogle ScholarPubMed
Bodis-Wollner, I. & Onofrj, M. (1987). The visual system in Parkinson's disease. In Parkinson's Disease, Advances in Neurology, Vol. 45, ed. Yahr, M.D. & Bergman, K.J., pp. 323–328. New York: Raven Press.Google Scholar
Bodis-Wollner, I. & Piccolino, M. (1988). Dopaminergic Mechanisms in Vision. New York: Alan R. Liss.Google Scholar
Bubenik, G.A. & Purtill, R.A. (1980). The role of melatonin and dopamine in retinal physiology. Canadian Journal of Physiology and Pharmacology 58, 1457–1462.CrossRefGoogle ScholarPubMed
Christensen, R.E., Pettit, T.H. & Barton, A.L. (1969). Retinal blood vessels and ocular blood flow. In The Retina Morphology, Function, and Clinical Characteristics, ed. Straatsma, B.R., Hall, M.O., Allen, R.A. & Crescitelli, F., pp. 411–441. Berkeley, California: University of California Press.Google Scholar
Cohen, A.I. & Blazynski, C. (1990). Dopamine and its agonists reduce a light-sensitive pool of cyclic AMP in mouse photoreceptors. Visual Neuroscience 4, 43–52.Google Scholar
Daw, N.W., Jensen, R.J. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neuroscience 13, 110–115.Google Scholar
Dickman, M. & Tran, V.T. (1990). D1 and D2 dopamine receptors are differentially localized in the rat retina. Investigative Ophthalmology and Visual Science (Suppl.) 31, 1622–80 (Abstract).Google Scholar
Farber, D.B., Flannery, J.G., Lolley, R.N. & Bok, D. (1985). Distribution patterns of photoreceptors, protein, and cyclic nucleotides in the human retina. Investigative Ophthalmology and Visual Science 26, 1558–1568.Google ScholarPubMed
Favard, C., Simon, A., Vigny, A. & Nguyen-Legros, J. (1990). Ultrastructural evidence of a close relationship between dopamine cell processes and blood capillary walls in Macaca monkey and rat retina. Brain Research 523, 127–133.Google Scholar
Harnois, C. & Di, Paolo T. (1990). Decreased dopamine in retina of Parkinsonian patients. Investigative Ophthalmology and Visual Science 4, 547–553.Google Scholar
Hogan, M.J., Alvarado, J.A. & Weddell, J.E. (1971). Histology of the Human Eye. Philadelphia, Pennsylvania: W.B. Saunders.Google Scholar
Leventhal, A.G., Ault, S.J. & Vitek, D.J. (1988). Retinal ganglion cell development in primates. Society for Neuroscience Abstracts 14, 188.6.Google Scholar
Mariani, A.P., Kolb, H. & Nelson, R. (1984). Dopamine-containing amacrine cells of the rhesus monkey retina parallel rods in spatial distribution. Brain Research 322, 1–7.CrossRefGoogle ScholarPubMed
Mariani, A.P., Neff, N.H. & Hadjiconstantinou, M. (1986). 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) treatment decreases dopamine and increases lipofuscin in mouse retina. Neuroscience Letters 72, 221–226.CrossRefGoogle ScholarPubMed
Missotten, L. (1974). Estimation of the ratio of cones to neurons in the fovea of the human retina. Investigative Ophthalmology and Visual Science 13, 1045–1049.Google ScholarPubMed
Mitrofanis, J., Vigny, A. & Stone, J. (1988). Distribution of catecholaminergic cells in the retina of the rat, guinea pig, cat, and rabbit. Independence from ganglion cell distribution. Journal of Comparative Neurology 267, 1–14.Google Scholar
Nettleship, E. (1875). Note on retinal blood vessels of the yellow spot. Royal London Ophthalmologic Hospital Reports 8, 269.Google Scholar
Nguyen-Legros, J. (1988). Morphology and distribution of catecholamine neurons in mammalian retina. In Progress in Retinal Research, Vol. 7, ed. Osborne, N. & Chader, G., pp. 113–147. Oxford: Pergamon Press.Google Scholar
Nguyen-Legros, J., Botteri, C., Le, Hoang P., Vigny, A. & Gay, M. (1984). Morphology of primate's dopaminergic amacrine cells as revealed by TH-like immunoreactivity on retinal flat-mounts. Brain Research 295, 145–153.Google Scholar
Nguyen-Legros, J. & Savy, C. (1988). Dopamine innervation of vertebrate retina: morphological studies. In Dopaminergic Mechanisms in Vision, Vol. 43, ed. Bodis-Wollner, I. & Piccolino, M., pp. 1–17. New York: Alan R. Liss.Google Scholar
Nguyen-Legros, J., Simon, A. & Sazdovitch, V. (1989). Physiopathologie du système dopaminergique rétinien dans la maladie de Parkinson. In Biologie Foundamentale et Clinique de la rétine, Vol. 1, ed. Christen, Y., Doly, M. & Droy-Lefaix, M.T., pp. 127–137. Heidelberg: Springer Verlag.Google Scholar
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
Nguyen-Legros, J. & Savy, C. (1990). Spatial organization of the DA innervation in the primate's fovea. Proceedings of the International Society for Eye Research, Vol. VI, 9th International Congress of Eye Research, Helsinki, pp. 234.Google Scholar
Osterberg, G. (1935). Topography of the layer of rods and cones in the human retina. Acta Ophthalmologica 6, 1–102.Google Scholar
Piccolino, M., Witkovsky, P. & Trimarchi, C. (1987). Dopaminergic mechanisms underlaying the reduction of electrical coupling between horizontal cells of the turtle retina induced by d-amphetamine, bicuculline, and veratridine. Journal of Neuroscience 7, 2273–2284.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University Chicago Press.Google Scholar
Rodieck, R.W. (1973). The Vertebrate Retina. Principles of Structure and Function. San Francisco, California: W.H. Freeman.Google 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.Google Scholar
Savy, C., Yelnik, J., Martin-Martinelli, E., Karpouzas, I. & Nguyen-Legros, J. (1989). Distribution and spatial geometry of dopamine interplexiform cells in the rat retina: I. Developing retina. Journal of Comparative Neurology 289, 99–110.Google Scholar
Schein, S.J. (1988). Anatomy of macaque fovea and spatial densities of neurons in foveal representation. Journal of Comparative Neurology 269, 479–505.CrossRefGoogle ScholarPubMed
Snodderly, D.M. & Weinhaus, R.S. (1990). Retinal vasculature of the fovea of the squirrel monkey, Saimiri sciureus: three-dimensional architecture, visual screening, and relationships to the neuronal layers. Journal of Comparative Neurology 297, 145–163.Google Scholar
Stone, J. & Johnston, E. (1981). The topography of primate retina: a study of the human, bushbaby, and new- and old-world monkey. Journal of Comparative Neurology 196, 205–223.CrossRefGoogle Scholar
Versaux-Botteri, C. & Nguyen-Legros, J. (1986). An improved method for tyrosine-hydroxylase immunolabelling of catecholamine cells in whole-mounted rat retina. Journal of Histochemistry and Cytochemistry 34, 734–748.Google Scholar
Versaux-Botteri, C., Martin-Martinelli, E., Nguyen-Legros, J., Geffard, M., Vigny, A. & Denoroy, L. (1986). Regional specialization of the rat retina: catecholamine-containing amacrine cell characterization and distribution. Journal of Comparative Neurology 243, 422–433.Google Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of AII amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle Scholar
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.Google Scholar