Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T17:35:13.577Z Has data issue: false hasContentIssue false
  • English
  • Français

Dopamine synthesis and metabolism in rhesus monkey retina: Development, aging, and the effects of monocular visual deprivation

Published online by Cambridge University Press:  02 June 2009

P. Michael Iuvone ,
Margarete Tigges ,
Alcides Fernandes  and
Johannes Tigges
P. Michael Iuvone
Affiliation:
Department of Pharmacology, Emory University, Atlanta Department of Ophthalmology, Emory University, Atlanta Yerkes Regional Primate Research Center (YRPRC), Emory University, Atlanta
Margarete Tigges
Affiliation:
Department of Anatomy and Cell Biology, Emory University, Atlanta Department of Ophthalmology, Emory University, Atlanta Yerkes Regional Primate Research Center (YRPRC), Emory University, Atlanta
Alcides Fernandes
Affiliation:
Yerkes Regional Primate Research Center (YRPRC), Emory University, Atlanta
Johannes Tigges
Affiliation:
Department of Anatomy and Cell Biology, Emory University, Atlanta Department of Ophthalmology, Emory University, Atlanta Yerkes Regional Primate Research Center (YRPRC), Emory University, Atlanta
Get access Rights & Permissions [Opens in a new window]

Abstract

The normal postnatal development, the influence of age, and the effects of visual deprivation on the dopamine system in the retina of rhesus monkeys were examined. The lowest level of retinal dopamine was found at birth. By 3–4 weeks of age, the dopamine concentration had more than doubled. This level remained relatively constant in the retinas of older infants and of adult monkeys up to 34 yr of age. The level of the dopamine metabolite 3,4-dihydroxyphenylacetic acid (DOPAC) and the activity of tyrosine hydroxylase did not significantly change as a function of age during the postnatal life span.

Monocular occlusion of newborn or infant monkeys for 1–15 months with opaque contact lenses resulted in decreases in the retinal concentrations of dopamine and DOPAC relative to the concentrations in the same animals' unoccluded eyes. Occlusion also resulted in a lower level of tyrosine hydroxylase activity in the retina. Monocular eyelid suture from birth to 15 months of age resulted in less consistent alterations of retinal dopamine and DOPAC levels; tyrosine hydroxylase activity, however, was consistently reduced by lid suture. Thus, dopamine synthesis and metabolism, and the ontogenetic increase of the retinal dopamine level of rhesus monkey are reduced by light deprivation.

Keywords

RetinaDopamineDevelopmentAgingVisual deprivationRhesus monkey
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 5 , May 1989 , pp. 465 - 471
Copyright
Copyright © Cambridge University Press 1989

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

Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: a role for post-receptoral neurons. In Progress in Retinal Research, Vol. 7, ed. Osborne, N. & Chader, G.J., pp. 21–61. Oxford: Pergamon Press.Google Scholar
Boatright, J.H., Hoel, M.H. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light and K+-evoked depolarization. Brain Research 482, 164–168.CrossRefGoogle ScholarPubMed
Bodis-Wollner, I. (1988). Altered spatio-temporal contrast vision in Parkinson's disease and MPTP treated monkeys: the role of dopamine. In Dopaminergic Mechanisms in Vision, ed. Bodis-Wollner, I. & Piccolino, M., pp. 205–220. New York: Alan R. Liss, Inc.Google Scholar
Cohen, J. & Neff, N.H. (1982). Retinal amacrine cell system tyrosine hydroxylase: the development of responsiveness to light and neuroleptic drugs. Developmental Brain Research 3, 160–163.CrossRefGoogle Scholar
Crawford, M.L.J. & Marc, R.E. (1976). Light transmission of cat and monkey eyelids. Vision Research 16, 323–324.CrossRefGoogle Scholar
DaPrada, M. (1977). Dopamine content and synthesis in retina and N. accumbens septi: pharmacological and light-induced modifications. Advances in Biochemical Psychopharmacology 16, 311–319.Google Scholar
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas. I. Induction of cone contraction is mediated by D2 receptors. Journal of Neurochemistry 46, 1006–1021.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1988). Dopaminergic regulation of lightand circadian-induced retinomotor movements in teleost fish. Proceedings of the International Society for Eye Research 5, 75.Google Scholar
DiPaolo, T., Harnois, C. & Daigle, M. (1987). Assay of dopamine and its metabolites in human and rat retina. Neuroscience Letters 74, 250–254.CrossRefGoogle Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system. I. Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London) 201, 7–26.Google Scholar
Dyer, R.S., Howell, W.E. & MacPhail, R.C. (1981). Dopamine depletion slows retinal transmission. Experimental Neurology 71, 326–340.CrossRefGoogle ScholarPubMed
Ehinger, B. (1966). Adrenergic nerves to the eye and to related structures in man and in cynamolgus monkey (Macaca irus). Investigative Ophthalmology 5, 42–52.Google Scholar
Fernandes, A., Tigges, M., Tigges, J., Gammon, J.A. & Chandler, C. (1988). Management of extended-wear contact lenses in infant rhesus monkeys. Behavior Research Methods, Instruments, and Computers 20, 11–17.CrossRefGoogle Scholar
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
Gammon, J.A., Boothe, R.G., Chandler, C.V., Tigges, M. & Wilson, J.R. (1985). Extended-wear soft contact lenses for vision studies in monkeys. Investigative Ophthalmology and Visual Science 26, 1636–1639.Google ScholarPubMed
Godley, B.F. & Wurtman, R.J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: effect of light stimulation. Brain Research 452, 393–395.CrossRefGoogle ScholarPubMed
Hamasaki, D.I., Trattler, W.B. & Hajek, A.S. (1986). Light on depresses and light off enhances the release of dopamine from the cat's retina. Neuroscience Letters 68, 112–116.CrossRefGoogle ScholarPubMed
Hedden, W.L. Jr. & Dowlino, 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
Iuvone, P.M. (1984). Calcium, ATP, and magnesium activate soluble tyrosine hydroxylase from rat striatum. Journal of Neurochemistry 43, 1359–1368.CrossRefGoogle ScholarPubMed
Iuvone, P.M. (1986 a). Neurotransmitters and neuromodulators in the retina: regulation, interactions, and cellular effects. In The Retina: A Model for Cell Biology Studies, Part II, ed. Adler, R. & Farber, D., pp. 1–72. Orlando: Academic Press.Google Scholar
Iuvone, P.M. (1986 b). Evidence for a D2 dopamine receptor in frog retina that decreases cyclic AMP accumulation and serotonin N-acetyltransferase activity. Life Sciences 38, 331–342.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Boatright, J.H. & Bloom, M.M. (1987). Dopamine mediates the light-evoked suppression of serotonin N-acetyltransferase activity in retina. Brain Research 418, 314–324.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Galli, C.L., Garrison-Gund, C.K. & Neff, N.H. (1978 a). Light stimulates tyrosine hydroxylase activity and dopa- mine synthesis in retinal amacrine neurons. Science 202, 901–902.CrossRefGoogle Scholar
Iuvone, P.M., Galli, C.L. & Neff, N.H. (1978 b). Retinal tyrosine hydroxylase: comparison of short-term and long-term stimulation by light. Molecular Pharmacology 14, 1212–1219.Google ScholarPubMed
Jensen, R.J. & Daw, N.W. (1988). Effects of dopaminergic agents on the activity of ganglion cells in the rabbit retina. In Dopaminergic Mechanisms in Vision, ed. Bodis-Wollner, I. & Piccolino, M., pp. 31–40. New York: Alan R. Liss, Inc.Google Scholar
Kato, S., Nakamura, T. & Negishi, K. (1980). Postnatal development of dopaminergic cells in the rat retina. Journal of Comparative Neurology 191, 227–236.CrossRefGoogle ScholarPubMed
Kramer, S.G. (1971). Dopamine: a retinal neurotransmitter. I. Retinal uptake, storage, and light stimulated release of H3-dopamine in vivo. Investigative Ophthalmology 10, 438–452.Google ScholarPubMed
Lam, D.M.K., Fung, S.-C. & Kong, Y.-C. (1981). Postnatal development of dopaminergic neurons in the rabbit retina. Journal of Neurosciencel, 1117–1132.CrossRefGoogle Scholar
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3025–3029.CrossRefGoogle ScholarPubMed
Laties, A. & Jacobowitz, D. (1966). A comparative study of the autonomic innervation of the eye of the monkey, cat, and rabbit. Anatomical Record 156, 383–386.CrossRefGoogle Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265–275.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform — horizontal cell system of the fish retina: effects of dopamine, light stimulation, and time in the dark. Proceedings of the Royal Society B (London) 231, 91–121.Google ScholarPubMed
Mariani, A.P. & Hokoc, J.N. (1988). Synaptic organization of dopaminergic amacrine cells in the rhesus monkey retina. In Dopaminergic Mechanisms in Vision, ed. Bodis-Wollner, I. & Piccolino, M., pp. 31–40. New York: Alan R. Liss, Inc.Google Scholar
Mariani, A.P., Kolb, H. & Nelson, R. (1984). Dopamine-containing amacrine cells of rhesus monkey retina parallel rods in spatial distribution. Brain Research 322, 1–7.CrossRefGoogle ScholarPubMed
McCulloch, J., Savaki, H.E., McCulloch, M.C. & Sokoloff, L. (1980). Retina-dependent activation by apomorphine of metabolic activity in the superficial layer of the superior colliculus. Science 207, 313–315.CrossRefGoogle ScholarPubMed
Melamed, E., Frucht, Y., Vidauri, J., Uzzan, A. & Rosenthal, J. (1986). The effect of postnatal light deprivation on the ontogenesis of dopamine neurons in rat retina. Developmental Brain Research 26, 280–284.CrossRefGoogle Scholar
Movshon, J.A. & Van Sluyters, R.C. (1981). Visual neural development. Annual Review of Psychology 32, 477–522.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J., Botteri, C., Phuc, L.H., Vigny, A. & Gay, M. (1984). Morphology of primate's dopaminergic amacrine cells as revealed by TH-Iike immunoreactivity on retinal flat mounts. Brain Research 295, 145–153.CrossRefGoogle ScholarPubMed
Osborne, N.N., Patel, S. & Vigny, A. (1984). Dopaminergic neurones in various retinas and the postnatal development of tyrosine-hydroxylase immunoreactivity in the rabbit retina. Histochemistry 80, 389–393.CrossRefGoogle ScholarPubMed
Parkinson, D. & Rando, R.R. (1983). Effects of light on dopamine metabolism in the chick retina. Journal of Neurochemistry 40, 39–46.CrossRefGoogle ScholarPubMed
Pierce, M.E. & Besharse, J.C. (1985). Orcadian regulation of retinomotor movements. I. Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671–689.CrossRefGoogle Scholar
Raviola, E. & Wiesel, T.N. (1985). An animal model of myopia. New England Journal of Medicine 312, 1609–1615.CrossRefGoogle ScholarPubMed
Reading, H.W. (1983). Dopaminergic receptors in bovine retina and their interaction with thyrotropin-releasing hormone. Journal of Neurochemistry 41, 1587–1595.CrossRefGoogle ScholarPubMed
Ryan, M.K. & Hendrickson, A.E. (1987). Interplexiform cells in macaque monkey retina. Experimental Eye Research 45, 57–66.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738–855.CrossRefGoogle ScholarPubMed
Stone, R.A., Laties, A.M., Raviola, E. & Wiesel, T.N. (1988). Increase in retinal vasoactive intestinal polypeptide after eyelid fusion in primates. Proceedings of the National Academy of Sciences of the U.S.A. 85, 257–260.CrossRefGoogle ScholarPubMed
Stone, R.A., Lin, T., Laties, A.M. & Iuvone, P.M. (1989). Retinal dopamine and form-deprivation myopia. Proceedings of the National Academy of Sciences of the U.S.A. 86, 704–706.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Tigges, J., Gordon, T.P., McClure, H.M., Hall, E.C. & Peters, A. (1988). Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. American Journal of Primatology 15, 263–273.CrossRefGoogle ScholarPubMed
Tigges, M., Hendrickson, A.E. & Tigges, J. (1984). Anatomical consequences of long-term monocular eyelid closure on lateral geniculate nucleus and striate cortex in squirrel monkey. Journal of Comparative Neurology 227, 1–13.CrossRefGoogle ScholarPubMed
Tigges, M., Iuvone, P.M., Tigges, J., Fernandes, A. & Gammon, J.A. (1987). Effects of monocular occlusion on lateral geniculate nucleus (LGN) anatomy and histochemistry, and on retinal dopamine system in infant rhesus monkeys. Society for Neuroscience Abstracts 13, 1535.Google Scholar
Troilo, D., Gottlieb, M.D. & Wallman, J. (1987). Visual deprivation causes myopia in chicks with optic nerve section. Current Eye Research 6, 993–999.CrossRefGoogle ScholarPubMed
Wallman, J., Gottlieb, M.D., Rajaram, V. & Fugate-Wentzek, L.A. (1987). Local retinal regions control local eye growth and myopia. Science 237, 73–77.CrossRefGoogle ScholarPubMed