Hostname: page-component-6d856f89d9-gndc8 Total loading time: 0 Render date: 2024-07-16T06:21:24.935Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunohistochemical localization of retinal serotonin cells in the lamprey (Lampetra fluviatilis)

Published online by Cambridge University Press:  02 June 2009

Claudine Botteri-Versaux ,
Najet Dalil ,
Natacha Kenigfest ,
Jacques Reperant ,
Nicolas Vesselkin  and
Jeanine Legros-Nguyen
Claudine Botteri-Versaux
Affiliation:
Laboratoire d'Anatomie Comparée, Museum National d'Histoire Naturelle, 55, rue Buffon 75005, Paris, France
Najet Dalil
Affiliation:
Laboratoire d'Anatomie Comparée, Museum National d'Histoire Naturelle, 55, rue Buffon 75005, Paris, France
Natacha Kenigfest
Affiliation:
Institut Sechenov-Leningrad, U.S.S.R.
Jacques Reperant
Affiliation:
Laboratoire d'Anatomie Comparée, Museum National d'Histoire Naturelle, 55, rue Buffon 75005, Paris, France INSERM U 106, Hospital La Salpêtrière, 750013, Paris, France
Nicolas Vesselkin
Affiliation:
Institut Sechenov-Leningrad, U.S.S.R.
Jeanine Legros-Nguyen
Affiliation:
Laboratoire de Neurocytologie Oculaire–INSERUM U 86, 15, rue de L'Ecole de Médecine 75006, Paris, France
Get access Rights & Permissions [Opens in a new window]

Abstract

Light-microscopic immunocytochemistry was used to study serotonin (5HT)-containing retinal cells in the lamprey (Lampetra fluviatilis). Observations of sections and flatmounted retinas enabled us to distinguish four principal types of 5HT-immunoreactive neurons, on the basis of the localization of their somata and the arrangement of their processes in the inner plexiform layer, (IPL). Type 1 cell bodies (9 μm mean diameter) were numerous and were found in the innermost row of the inner nuclear layer (INL). They sent their processes into a dense plexus in sublamina a of the IPL. Type 2 cell bodies (12 μm mean diameter) were observed near the inner limiting membrane, their processes forming a plexus in sublamina b of the IPL. Most of the type 3 cells were bistratified, their cell bodies (similar in dimension to type 1) were located in the INL and their dendrites projected to both plexuses. Type 4 cell bodies (15 μm mean diameter) were observed in the middle of the IPL and could be compared with the interstitial described elsewhere. Their processes probably ended in the 5HT plexus of sublamina b but because of their sinuous course in the IPL, we could not affirm this fact. Most of 5HT immunoreactive cells were thought to be amacrine cells, but the presence of some thin processes emerging either from the soma or the primary dendrite, principally in type 1 and 2 cells, raises the possibility that some ganglion cells could be 5HT immunoreactive. The organization of the 5HT processes into two plexuses located in sublaminae a and b of the IPL resemble the functional ON and OFF pathway seen in the other vertebrates.

Keywords

SerotoninRetinaLampreyImmunocytochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 3 , September 1991 , pp. 171 - 177
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

Blazynski, C., Ferrendelli, J.A. & Cohen, A.I. (1985). Indoleamine-sensitive adenylate cyclase in rabbit retina. Journal of Neurochemistry 45, 440–447.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.M. (1986). 5HT2 antagonist reduces ON responses in the rabbit retina. Brain Research 384, 161–165.CrossRefGoogle ScholarPubMed
Brunken, W.J., Witkovsky, P. & Karten, H.J. (1986). Retinal neurochemistry of three elasmobranch species. An immunohistochemical approach. Journal of Comparative Neurology 243, 1–12.CrossRefGoogle ScholarPubMed
Bruun, A., Ehinger, B. & Sytsma, V.M. (1984). Neurotransmitter localization in the skate retina. Brain Research 295, 233–248.CrossRefGoogle ScholarPubMed
Cajal, S.R. Y (1911). Appareil visuel. Rétine ou organe récepteur de l'excitation visuelle. In Histologie du Système Nerveuxde I'Homme et des Vertébrés, Tome II, ed. Cajal, S.R. Y., pp. 296–325. Madrid: Consejo Superior de Investigaciones Cientificas Instituto Ramon y Cajal.Google Scholar
Cutcliffe, N. & Osborne, N.N. (1987). Serotoninergic and cholinergic stimulation of inositol phosphate formation in rabbit retina. Evidence for the presence of 5HT2 and muscarinic receptors. Brain Research 421, 95–104.CrossRefGoogle Scholar
Dacey, D. (1985). Wide spreading terminal axons in the inner plexiform layer of the cat's retina: evidence for intrinsic axon collaterals of ganglion cells. Journal of Comparative Neurology 242, 247–262.CrossRefGoogle ScholarPubMed
Daw, N.W., Jensen, R.J. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neuroscience 13, 110–115.CrossRefGoogle ScholarPubMed
de Miguel, E. & Wagner, H.J. (1990). Tyrosine hydroxylase immunoreactive interplexiform cells in the lamprey retina. Neuroscience Letters 113, 151–155.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A. & Vallerga, S. (1989). Structure-function correlation in amacrine cells of fish and amphibian retinae. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 195–208. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system, 1-Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London) 201, 7–26.Google Scholar
Ehinger, B. (1976). Biogenic monoamines as transmitters in the retina. In Transmitters of the Visual Process, ed. Bouting, S.L., pp. 145–163. Oxford: Pergamon.CrossRefGoogle Scholar
Ehinger, B., Holmberg, K. & Ohman, P. (1977). Aminergic and indoleamine accumulating neurons in the retina of the river lamprey. Acta Zoologica (Stockholm) 58, 117–123.Google Scholar
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of “ON” and “OFF” pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Hinds, J.W. & Hinds, P.L. (1983). Development of retinal amacrine cells in the mouse embryo: evidence for two modes of formation. Journal of Comparative Neurology 213, 1–23.CrossRefGoogle ScholarPubMed
Holmgren-Taylor, I. (1983a). Synaptic organization of the indoleamine-accumulating neurons in the cyprinid retina. Cell and Tissue Research 229, 317–335.Google ScholarPubMed
Holmgren-Taylor, I. (1983b). Synapses of the inner plexiform layer in the retina of cyprinid fish. Cell and Tissue Research 229, 337–350.Google ScholarPubMed
Kato, S., Teranishi, T., Kuo, C.H. & Negishi, K. (1982). 5-hydroxy-tryptamine stimulates [3H]-dopamine release from the fish retina. Journal of Neurochemistry 39, 493–498.CrossRefGoogle ScholarPubMed
Marc, R.E. (1982). Spatial organization of neurochemically classified interneurones of Goldfish retina. 1-local pattern, Vision Research 22, 589–602.CrossRefGoogle Scholar
Marc, R.E., Liu, W.-L.S., Scholz, K. & Muller, J.F. (1988). Serotoninergic and serotonin-accumulating neurons in the goldfish retina. Journal of Neuroscience 8, 3427–3450.CrossRefGoogle Scholar
Martin-Martinelli, E. (1988). Evolution de la morphologie et de la distribution des neurones catecholaminergiques dans la rétine du rat albinos au cours du développement postnatal. Thèse de Doctorat, University of Paris VI.Google Scholar
Millar, T.J. & Morgan, I.G. (1989). Serotoninergic cells in the chicken retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & OsBorne, N.N., pp. 445–453. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Negishi, K., Kato, S. & Teranishi, T. (1982). Dopaminergic cells of river lamprey retina revealed by histofluorescence study. Acta of Histochemistry and Cytochemistry 15, 757–767.CrossRefGoogle Scholar
Negishi, K., Kiyama, H., Kato, S., Teranishi, T., Hatakenaka, S., Katayama, Y., Miki, N. & Tohyama, M. (1986). An immunohisto-chemical study on the river lamprey retina. Brain Research 362, 389–393.CrossRefGoogle Scholar
Negishi, K. & Teranishi, T. (1989). Dendritic morphology of a class of interstitial amacrine cells in carp retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 133–143. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Nguyen-Legros, J. (1988). Morphology and distribution of catecholamine neurons in mammalian retina. In Progress in Retinal Research, Vol. 7, ed. Osborne, N.N. & Chader, J., pp. 113–147. Oxford: Pergamon Press.Google Scholar
Osborne, N.N., Nesselhut, T., Nicholas, D.A. & Cuello, A.C. (1981). Serotonin: a transmitter candidate in vertebrate retina. Neurochemistry International 3, 171–176.CrossRefGoogle ScholarPubMed
Osborne, N.N. (1982). Uptake, localization and release of serotonin in the chick retina. Journal of Physiology (London) 331, 469–479.Google Scholar
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotoninergic neurones of the retina. In Progress in Retinal Research, Vol. 3, ed. Osborne, N.N. & Chader, J., pp. 61–103. Oxford: Pergamon Press.Google Scholar
Piccolino, M. & Demontes, G. (1988). Dopaminergic system and modulation of electrical transmission between horizontal cells in the turtle retina. In Neurology and Neurobiology—Dopaminergic Mechanisms in Vision, Vol. 43, ed. Bodis-Wollner, I. & Piccolino, M., pp. 137–162. New York: Alan R. Liss.Google Scholar
Sternberger, L.A. (1979). Immunocytochemistry. New York: John Wiley.Google ScholarPubMed
Thier, P. & Wässle, H. (1984). Indoleamine mediated reciprocal modulation of ON-centre and OFF-centre ganglion cell activity in the retina of the cat. Journal of Physiology (London) 351, 313–630.Google Scholar
Tornqvist, K., Hansson, C. & Ehinger, B. (1983). Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochemistry International 5, 299–308.CrossRefGoogle ScholarPubMed
Tretjakoff, D.K. (1916). The sense organs of the lamprey (Lampetra fluviatilis). University of Novorossijsk, Odessa.Google Scholar
Versaux-Botteri, C., Kenigfest, N.B., Dalil, N., Repérant, J., Vesselkin, N.P. & Nguyen-Legros, J. (1990). Localization of serotonin-immunoreactive cells in the lamprey retina. 10th European Winter Conference on Brain Research, Les Arcs-France (abstract).Google Scholar
Vesselkin, N.P., Repérant, J., Kenigfest, N.B., Rio, J.P., Miceli, D. & Shupliakov, O.V. (1989). Centrifugal innervation of the lamprey retina. Light and electron microscopic and electrophysiological investigations. Brain Research 493, 51–65.CrossRefGoogle ScholarPubMed
Villar, M.J., Vitale, M.L. & Parisi, M.N. (1987). Dorsal raphe serotonergic projection of the retina. A combined peroxidase tracing-neurochemical/high-performance liquid chromatography study in the rat. Neuroscience 22, 681–686.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985). Morphological and pharmacological analysis of putative bipolar and amacrine cells in the retina of a turtle, Pseudemys scripta elegans. Cell and Tissue Research 241, 373–382.CrossRefGoogle ScholarPubMed
Weiler, R. & Ammermüller, J. (1986). Immunocytochemical localization of serotonin in intracellularly analyzed and dye injected ganglion cells of the turtle retina. Neuroscience Letters 72, 147–152.CrossRefGoogle ScholarPubMed
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine-and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217–225.CrossRefGoogle ScholarPubMed
Yang, S.Z., Lam, D.M. & Watt, C.B. (1989). Localization of serotonin like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 287, 28–37.CrossRefGoogle Scholar