Summary
Two types of amacrine cell immunoreactive for tyrosine hydroxylase, the rate-limiting enzyme in the catecholamine synthetic pathway, are present in the retina of the rhesus monkey,Macaca mulatta. The well-known dopaminergic, or type 1 catecholamine amacrine cells have relatively large cell bodies almost exclusively in the inner nuclear layer with processes that densely arborize in the outermost stratum of the inner plexiform layer and fine, radially-oriented fibres in the inner nuclear layer. Type 2 catecholamine amacrine cells, in contrast, have smaller cell bodies in the inner nuclear layer, the inner plexiform layer and the ganglion cell layer, and have sparsely-branching processes ramifying in the centre of the inner plexiform layer. Although type 2 catecholamine cells are more numerous than type 1 catecholamine amacrines, type 2 cells contain less than one-third the amount of tyrosine hydrolase as the type 1 cells. Electron microscopy of retinal tissue immunoreacted for tyrosine hydrolase by the peroxidase-antiperoxidase method revealed synaptic input from amacrine cells at conventional synapses, and bipolar cells at ribbon synapses onto the type 2 catecholamine amacrine cells. Curiously, although the synaptic input is comparatively easily found, the output synapses, or synapses of the type 2 catecholamine amacrine cells onto other neuronal elements, are rarely found. Some synapses of the type 2 catecholamine cells onto non-immunoreactive amacrine cells have been identified, however. This unusual pattern of synaptic organization, with many identifiable input synapses but few morphologically characterizable output synapses, suggests a paracrine function for the dopamine released by the type 2 catecholamine amacrine cells in the primate retina.
Similar content being viewed by others
References
Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study.Brain Research 9, 268–87.
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, 1006–21.
Dowling, J. E. &Boycott, B. B. (1986) Organization of the primate retina: electron microscopy.Proceedings of the Royal Society of London, Series B 166, 80–111.
Dowling, J. E. &Ehinger, B. (1975) Synaptic organization of the amine-containing interplexiform cells of the goldfish and cebus monkey retinas.Science 188, 270–3.
Ehinger, B. (1966) Adrenergic nerves to the eye and to related structures in man and in the cynomolgus monkey (Macaca irus).Investigative Ophthalmology 5, 42–52.
Ehinger, B. (1982) Neurotransmitter systems in the retina.Retina 2, 305–21.
Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study.Journal of Anatomy 93, 420–33.
Hadjiconstantinou, M., Mariani, A. P., Panula, P., Joh, T. H. &Neff, N. H. (1984) Immunohistochemical evidence for epinephrine-containing retinal amacrine cells.Neuroscience 13, 547–51.
Hokoc, J. N. &Mariani, A. P. (1987) Tyrosine hydroxylase immunoreactivity in the rhesus monkey retina reveals synapses from bipolar cells to dopaminergic amacrine cells.Journal of Neuroscience 7, 2785–93.
Iuvone, P. M. (1988) Dopamine: a light-adaptive modulator of melatonin synthesis in the frog retina. InDopaminergic Mechanisms in Vision (edited byBodis-Wollner, I. &Piccolino, M.) pp. 95–107. New York: Alan R. Liss.
Iuvone, P. M., Tigges, M., Fernandes, A. &Tigges, J. (1989) Dopamine synthesis and metabolism in rhesus monkey retina: development, aging, and the effects of monocular deprivation.Visual Neuroscience 2, 465–71.
Keyser, K. T., Karten, H. J., Katz, B. &Bohn, M. C. (1987) Catecholaminergic horizontal and amacrine cells in the ferret retina.Journal of Neuroscience 7, 3996–4004.
Kolb, H. &Famiglietti, E. V. Jr. (1983) Rod and cone pathways in the inner pléxiform layer of cat retina.Science 186, 47–9.
Laties, A. M. &Jacobowitz, D. (1966) A comparative study of the autonomic innervation of the eye in monkey, cat and rabbit.Anatomical Record 156, 383–96.
Mariani, A. P. (1983) Giant bistratified bipolar cells in monkey retina.Anatomical Record 206, 215–20.
Mariani, A. P. &Hokoc, J. N. (1988) Two types of tyrosine hydroxylase immunoreactive amacrine cell in the rhesus monkey retina.Journal of Comparative Neurology 276, 81–91.
Mariani, A. P., Kolb, H. &Nelson, R. (1984) Dopaminecontaining amacrine cells of rhesus monkey retina parallel rods in spatial distribution.Brain Research 322, 1–7.
McMahon, D. G., Knapp, A. G. &Dowling, J. E. (1989) Horizontal cell gap junctions: single-channel conductance and modulation by dopamine.Proceedings of the National Academy of Science (USA) 86, 7639–43.
Nguyen-Legros, J., Botteri, C., Phuc, L. H., 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, 145–53.
Nguyen-Legros, J., Versaux-Botteri, C., Vigny, A. &Raux, N. (1985) Tyrosine hydroxylase immunohisto-chemistry fails to demonstrate dopaminergic interplexiform cells in the turtle retina.Brain Research 339, 323–8.
Piccolino, M., Neyton, J. &Gerschenfeld, H. M. (1984) Decrease of gap junction permeability induced by cyclic adenosine 3′5′-monophosphate in horizontal cells of the turtle retina.Proceedings of the National Academy of Sciences (USA) 79, 3671–5.
Stell, W. K., Walker, S. E., Chohan, K. S. &Ball, A. K. (1984) The goldfish nervus terminalis: a lutenizing hormone-releasing hormone and molluscan cardioexcitatory peptide immunoreactive olfactoretinal pathway.Proceedings of the National Academy of Sciences (USA) 81, 940–4.
Sternberger, L. (1986)Immunocytochemistry, 3rd edn. New York: Wiley.
Tauchi, M., Madigan, N. K. &Masland, R. H. (1990) Shapes and distributions of the catecholamine-accumulating neurons in the rabbit retina.Journal of Comparative Neurology 293, 178–89.
Teitleman, G., Gershon, M. D., Rothman, T. P., Joh, T.-H. &Reis, D. J. (1981) Proliferation and distribution of cells that transiently express a catecholaminergic phenotype during development in mice and rats.Developmental Biology 86, 348–55.
Teranishi, T., Negishi, K. &Kato, S. (1983) Dopamine modulates S-potential and dye-coupling between external horizontal cells in carp retina.Nature 301, 243–6.
Wang, H.-H., Cuenca, N. &Kolb, H. (1990) Development of morphological types and distribution patterns of amacrine cells immunoreactive to tyrosine hydroxylase in the cat retina.Visual Neuroscience 4, 159–75.
Yazulla, S. &Zucker, C. L. (1988) Synaptic organization of dopaminergic interplexiform cells in the goldfish retina.Visual Neuroscience 1, 13–29.
Zucker, C. L. &Dowling, J. E. (1987) Centrigufal fibres synapse on dopaminergic interplexiform cells in teleost retina.Nature 330, 166–8.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mariani, A.P. Synaptic organization of type 2 catecholamine amacrine cells in the rhesus monkey retina. J Neurocytol 20, 332–342 (1991). https://doi.org/10.1007/BF01235550
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01235550