Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-11T05:29:27.237Z Has data issue: false hasContentIssue false
  • English
  • Français

Maturation of somatostatin immunoreactivity in the pigeon retina: Morphological characterization and quantitative analysis

Published online by Cambridge University Press:  02 June 2009

Giovanna Traina ,
Gigliola Fontanesi  and
Paola Bagnoli
Giovanna Traina
Affiliation:
Department of Environmental Sciences, University of Tuscia, Viterbo, Italy
Gigliola Fontanesi
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, Italy
Paola Bagnoli
Affiliation:
Department of Environmental Sciences, University of Tuscia, Viterbo, Italy
Get access Rights & Permissions [Opens in a new window]

Abstract

In addition to a modulatory function, somatostatin (SS) is likely to exert a morphogenetic and/or trophic role in the developing nervous system. In this study, a mouse monoclonal antibody directed to SS was used to investigate the posthatching development of SS-immunoreactivity (SS-ir) in the pigeon retina to provide a basis for a better understanding of the role of this peptide in retinal maturation. In the adult, SS-ir was observed in amacrine cells located in the inner nuclear layer (INL) of the entire retina. Two cell types were recognized according to their morphology. They showed a differential density distribution. Cell type indicated as “adult 1” (AD1) was characterized by pear-shaped cell bodies with single primary processes directed to the inner plexiform layer (IPL) and was mostly present in the red field. In contrast, cell type indicated as “adult 2” (AD2) was characterized by round-shaped somata with 1–3 primary processes and was highly represented in the fovea and the dorsal periphery. Posthatching maturation of the pigeon retina was characterized by drastic changes in the pattern of SS-ir. Over the first days posthatching, SS-ir was observed in sparsely distributed somata mostly located in the ganglion cell layer (GCL). This cell type indicated as “hatch” (H) was characterized by dense granular staining and became extremely rare at 7 days. Over the same period, growing SS-positive axons displaying enlarged growth cones were found in the optic tract (TrO). These observations suggest the possibility that ganglion cells transiently expressing SS are present at early stages of posthatching development. Of the two types of SS-containing cells observed in the adult, the first to be recognized morphologically was cell type AD1 which appeared at 2 days after hatching in the INL. These cells were virtually adult-like in morphology by 7 days. In contrast, cell type AD2 was not apparent until 7 days posthatching. The density (defined as number of cells/mm2 of retinal tissue) and the total number of SS-containing cells changed during posthatching maturation. In particular, the adult number of cell type AD1 was reached at about 10 days, while the number of cell type AD2 was reached at about 3 weeks posthatching. At this stage, both cell types also displayed their mature density distribution. The present findings suggest a temporal relationship between the maturation of SS-ir and developmental events which include the onset of light-driven activity and the maturation of retinal acuity. Our results also demonstrate significant differences in the pattern of SS-ir between the avian and the mammalian retina and suggest that SS-containing neurons represent important intraretinal association neurons in the retina of birds.

Keywords

Retinal amacrine cellsGanglion cellsPeptidesDevelopment
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 165 - 177
Copyright
Copyright © Cambridge University Press 1994

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

Bagnoli, P., Casini, G., Fontanesi, G. & Sebastiani, L. (1989 a). Reorganization of visual pathways following posthatching removal of one retina in pigeons. Journal of Comparative Neurology 288, 512–527.CrossRefGoogle ScholarPubMed
Bagnoli, P., Fontanesi, G., Streit, P., Domenici, L. & Alesci, R. (1989b). Changing distribution of GABA-like immunoreactivity in pigeon visual areas during the early posthatching period and effects of retina removal on tectal GABAergic system. Visual Neuroscience 3, 491–508.CrossRefGoogle Scholar
Bagnoli, P., Fontanesi, G., Alesci, R. & Erichsen, J.T. (1992). Distribution of neuropeptide Y, substance P and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. Journal of Comparative Neurology 318, 392–414.CrossRefGoogle ScholarPubMed
Bagnoli, P., Porciatti, V., Fontanesi, G. & Sebastiani, L. (1987). Morphological and functional changes in the retinotectal system of the pigeon during the early posthatching period. Journal of Comparative Neurology 256, 400–411.CrossRefGoogle ScholarPubMed
Bagnoli, P., Porciatti, V., Lanfranchi, A. & Bedini, C. (1985). Developing pigeon retina. Light evoked responses and ultrastructure of outer segments and synapses. Journal of Comparative Neurology 235, 384–394.CrossRefGoogle ScholarPubMed
Bagnoli, P., Di Gregorio, S., Molnar, M., Romei, C. & Fontanesi, G. (1991). Maturation and plasticity of neuropeptides in the visual system. In The Changing Visual System, ed. Bagnoli, P. & Hodos, W., pp. 185–197. New York: Plenum Press.CrossRefGoogle Scholar
Bodenant, C., Leroux, P., Gonzales, B.J. & Vaudry, H. (1991). Transient expression of somatostatin receptors in the rat visual system during development. Neuroscience 41, 595–606.CrossRefGoogle ScholarPubMed
Brecha, N., Casini, G. & Rickman, D.W. (1991). Organization and development of sparsely distributed wide-field amacrine cells in the rabbit retina. In The Changing Visual System, ed. Bagnoli, P. & Hodos, W., pp. 95–117. New York: Plenum Press.CrossRefGoogle Scholar
Brecha, N., Karten, H.J. & Schenker, C. (1981). Neurotensin-like and somatostatin-like immunoreactivity within amacrine cells of the retina. Neuroscience 6, 1329–1340.CrossRefGoogle ScholarPubMed
Brink-Larsen, J.N., Bersani, M., Olcese, J., Holst, J.J. & Moller, M. (1990). Somatostatin and prosomatostatin in the retina of the rat: An immunohistochemical, in situ hybridization and chromatographic study. Visual Neuroscience 5, 441–452.CrossRefGoogle Scholar
Buchan, A.M.J., Sikora, L.K.J., Levy, J.G., McIntosh, C.H.S., Dyck, I. & Brown, J.C. (1985). An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83, 175–183.CrossRefGoogle ScholarPubMed
Bulloch, A.G.M. (1987). Somatostatin enhances neurite outgrowth and electrical coupling of regenerating neurons in Helisoma. Brain Research 412, 6–17.CrossRefGoogle ScholarPubMed
Catsicas, S., Catsicas, M. & Clarke, P.G.H. (1987). Long-distance intraretinal connections in birds. Nature 326, 186–187.CrossRefGoogle ScholarPubMed
Chun, J.J.M., Nakamura, M.J. & Shatz, C.J. (1987). Transient cells of the developing telencephalon are peptide-immunoreactive neurons. Nature 325, 617–620.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge: Belknap Press, pp. 1–12.Google Scholar
Ferriero, D.M. (1992). Developmental expression of somatostatin receptors in the rat retina. Developmental Brain Research 67, 309–315.CrossRefGoogle ScholarPubMed
Ferriero, D.M. & Sagar, S.M. (1987). Development of somatostatin immunoreactive neurons in rat retina. Developmental Brain Research 34, 207–214.CrossRefGoogle Scholar
Ferriero, D.M., Head, V.A., Edwards, R.H. & Sagar, S.M. (1990). Somatostatin mRNA and molecular forms during development of rat retina. Developmental Brain Research 57, 15–19.CrossRefGoogle ScholarPubMed
Fontanesi, G., Traina, G. & Bagnoli, P. (1993). Somatostatin-like immunoreactivity in the pigeon visual system: Developmental expression and effects of retina removal. Visual Neuroscience 10, 271–285.CrossRefGoogle ScholarPubMed
Fontanesi, G., Traina, G., Molnar, M. & Bagnoli, P. (1992). Somatostatin expression and plasticity in the pigeon visual system. Neuroscience Abstracts 18, 328.11.Google Scholar
Gonzalez, B.J., Leroux, B., Boer, G.J. & Vaudry, H. (1990). Expression of somatostatin receptors is impaired in the cerebellum of developing Brattleboro rats. Brain Research 532, 115–119.CrossRefGoogle ScholarPubMed
Gotow, T., Williams, T.H., Jew, J.Y., Cassell, M.D., Palkovits, M. & Hashimoto, P.H. (1989). Collateral sprouting of somatostatin-immunoreactive axons after partial deafferentation of the central nucleus of the rat amygdala. Brain Research 492, 325–336.CrossRefGoogle ScholarPubMed
Grimm-Jorgesen, Y. (1987). Somatostatin and calcitonin stimulate neurite regeneration of molluscan neurons in vitro. Brain Research 403, 121–126.CrossRefGoogle Scholar
Hamano, K., Katayama-Kumoi, Y., Kiyama, H., Ishtmoto, I., Manabe, R. & Tohyama, M. (1989). Coexistence of enkephalin and somatostatin in the chicken retina. Brain Research 489, 254–260.CrossRefGoogle ScholarPubMed
Hayashi, M. (1992). Ontogeny of some neuropeptides in the primate brain. Progress in Neurobiology 38, 231–360.CrossRefGoogle ScholarPubMed
Hayes, B.P., Hodos, W., Holden, A.L. & Low, J.C. (1987). The projection of the visual field upon the retina in the pigeon. Vision Research 27, 31–40.CrossRefGoogle ScholarPubMed
Hokfelt, T. (1991). Neuropeptides in perspective: The last ten years. Neuron 7, 867–879.CrossRefGoogle ScholarPubMed
Ishimoto, I., Millar, T., Chubb, W. & Morgan, I.G. (1986). Soma-tostatin-immunoreactive amacrine cells of chicken retina: Retinal mosaic, ultrastructural features and light-driven variations in peptide metabolism. Neuroscience 17, 1217–1233.CrossRefGoogle ScholarPubMed
Kagami, H., Sakai, H., Uryu, K., Kaneda, T. & Sakanaka, M. (1991). Development of tyrosine hydroxylase-like immunoreactive structures in the chick retina: Three-dimensional analysis. Journal of Comparative Neurology 308, 356–370.CrossRefGoogle ScholarPubMed
Karten, H.J. & Hodos, W. (1967). A stereotaxic atlas of the brain of the pigeon (Columba livia), Baltimore, Maryland: The Johns Hopkins Press.Google Scholar
Kentroti, S. & Vernadakis, A. (1990). Growth hormone-releasing hormone and somatostatin influence neuronal expression in developing chick brain. II. Cholinergic neurons. Brain Research 512, 297–303.CrossRefGoogle ScholarPubMed
Li, H.-B., Watt, C.B. & Man-Kit Lam, D. (1990). Double-label analysis of somatostatin's coexistence with enkephalin and gamma-ami-nobutyric acid in amacrine cells of the chicken retina. Brain Research 525, 304–309.CrossRefGoogle Scholar
Mariani, A.P. (1982). Association amacrine cells could mediate directional selectivity in pigeon retina. Nature 298, 654–655.CrossRefGoogle ScholarPubMed
Marshak, D.W. (1992). Peptidergic neurons of teleost retinas. Visual Neuroscience 8, 137–144.CrossRefGoogle ScholarPubMed
Mitrofanis, J., Robinson, S.R. & Provis, J.M. (1989). Somatostatin-ergic neurons of the developing human and cat retinae. Neuroscience Letters 104, 209–216.CrossRefGoogle ScholarPubMed
Morgan, I.G., Oliver, J. & Chubb, I.W. (1983). The development of amacrine cells containing somatostatin-like immunoreactivity in chicken retina. Developmental Brain Research 8, 71–76.CrossRefGoogle Scholar
Nalbach, H.O., Wolf-Oberhollenzer, F. & Kirschfeld, D. (1990). The pigeon’s eye viewed through an ophthalmoscopic microscope: Orientation of retinal landmarks and significance of eye movements. Vision Research 30, 529–540.CrossRefGoogle ScholarPubMed
Porciatti, V., Bagnoli, P., Lanfranchi, A. & Bedini, C. (1985). Interaction between photoreceptors and pigment epithelium in developing pigeon retina: An electrophysiological and ultrastructural study. Documenta Ophthalmology 60, 413–419.CrossRefGoogle ScholarPubMed
Rager, G.H. (1980). Advances in Anatomy, Embryology and Cell Biology: Development of the Retinotectal Projection in the Chicken. Berlin/Heidelberg: Springer.Google ScholarPubMed
Rager, G. & Rager, U. (1978). Systems-matching by degeneration. A quantitative electron-microscopic study of the generation and degeneration of retinal ganglion cells in the chicken. Experimental Brain Research 33, 65–78.CrossRefGoogle ScholarPubMed
Rickman, D.W. & Brecha, N. (1989). Morphologies of somatostatin-immunoreactive neurons in the rabbit retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N., pp. 461–468. New York: Springer-Verlag.CrossRefGoogle Scholar
Sagar, S.M. & Marshall, P.E. (1988). Somatostatin-like immunoreactive material in associational ganglion cells of human retina. Neuroscience 27, 507–516.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.CrossRefGoogle Scholar
Walker, S.E. & Stell, W.K. (1986). Gonadotropin-releasing hormone (GnRH), molluscan cardioexcitatory peptide (FMR amide), enkephalin and related neuropeptides affect goldfish ganglion cell activity. Brain Research 384, 262–273.CrossRefGoogle Scholar
Watt, C.B., Li, H.-B., & Man-Kit Lam, D. (1985). The presence of three neuroactive peptides in putative glycinergic amacrine cells of an avian retina. Brain Research 348, 187–191.CrossRefGoogle ScholarPubMed
White, C.A. & Chalupa, L.M. (1991). Subgroup of alpha ganglion cells in the adult cat retina is immunoreactive for somatostatin. Journal of Comparative Neurology 304, 1–13.CrossRefGoogle ScholarPubMed
White, C.A. & Chalupa, L.M. (1992). Ontogeny of somatostatin immunoreactivity in the cat retina. Journal of Comparative Neurology 317, 129–144.CrossRefGoogle ScholarPubMed
White, C.A., Chalupa, L.M., Johnson, D. & Brecha, N.C. (1990). Somatostatin-immunoreactive cells in the adult cat retina. Journal of Comparative Neurology 293, 134–150.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of somatostatin in the rabbit retina. Journal Neuroscience 10, 383–393.CrossRefGoogle ScholarPubMed