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Ultrastructural and histochemical studies of the rat iris: identified neuronal inputs and supportive glia

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Journal of Neurocytology

Summary

A detailed ultrastructural description was made of the rat iris with special emphasis on nerve fibre populations and their supportive glial cells. The location and identity of different autonomic (sympathetic and parasympathetic) and sensory nerves was further studied by monoamine histofluorescence, acetylcholinesterase histochemistry, immunohistochemistry for substance P and neurofilament, and Linder's silver staining. Schwann cells were defined with immunohistochemical techniques using antiserum to glial fibrillary acidic protein. By correlation of these morphological techniques, the relative proportion of different neuronal inputs and their glial constituents in various parts of the rat iris could be determined. The sympathetic and parasympathetic unmyelinated fibres showed the well-known preferential localization in the posterior part, approaching the smooth muscle cells and chromatophores in the dilator muscle. Larger arterioles in the anterior loose stroma of the iris were in close proximity to sympathetic fibres as indicated by monoamine histofluorescence. Sensory trigeminal nerves were visualized both with Linder's silver staining and neurofilament immunohistochemistry. Large myelinated axon bundles in the anterior part of the iris were clearly seen, and thin unmyelinated fibres were scattered throughout the anterior and posterior parts. Unmyelinated substance P-containing fibres were scattered preferentially in the anterior part of the iris, without close association with blood vessels. Distribution of supportive cells, indicated by means of immunofluorescence with antiserum against glial fibrillary acidic protein, appeared largely similar to that of neurofilament-positive nerve fibres. In the sphincter muscle, cholinesterase-positive nerve fibres were densely packed and adrenergic fibres as well as sensory, neurofilament- and substance P-containing fibres were sparse but distributed throughout the muscle. Accompanying glial cells positive for glial fibrillary acidic protein were also found.

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References

  • Ayer-Lelievre, C. S., Granholm, A.-Ch. &Seiger, Å. (1984) Silver impregnation of intrinsic sensory innervation of rat iris in toto.Journal of Anatomy (in press).

  • Björklund, H., Dahl, D., Olson, L. &Seiger, Å. (1984a) GFA-like immunoreactivity in the iris. Development, distribution and reactive changes following transplantation.Journal of Neuroscience 4, 978–88.

    PubMed  Google Scholar 

  • Björklund, H., Hoffer, B., Olson, L., Palmer, M. &Seiger, Å. (1984b) Enkephalin immunoreactivity in iris nerves: Distribution in normal and grafted irides, persistence and enhanced fluorescence after denervations.Histochemistry 80, 1–7.

    PubMed  Google Scholar 

  • Björklund, H., Olson, L. &Seiger, Å. (1983) Enkephalin-like immunofluorescence in nerves of the rat iris following systemic capsaicin injection.Medical Biology 61, 280–2.

    PubMed  Google Scholar 

  • Coons, A. H. (1958) Fluorescent antibody methods. InGeneral Cytochemical Methods (edited byDanielli, J. F.), pp. 399–422. New York: Academic Press.

    Google Scholar 

  • Corrodi, H. &Jonsson, G. (1967) The formaldehyde fluorescence method for the histochemical demonstration of biogenic monoamines. A review on the methodology.Journal of Histochemistry and Cytochemistry 15, 65–78.

    Google Scholar 

  • Costa, M., Buffa, R., Furness, J. B. &Solcia, E. (1980) Immunohistochemical localization of polypeptides in peripheral autonomie nerves using whole mount preparations.Histochemistry 65, 157–65.

    PubMed  Google Scholar 

  • Costa, M., Patel, Y., Furness, J. B. &Arimura, A. (1977) Evidence that some intrinsic neurons of the intestine contain somatostatin.Neuroscience Letters 6, 215–22.

    Google Scholar 

  • Cuello, A. C., Del Fiacco, M. &Paxinos, G. (1978) The central and peripheral ends of the substance P-containing sensory neurons in the rat trigeminal system.Brain Research 152, 499–509.

    PubMed  Google Scholar 

  • Dahl, D. &Bignami, A. (1976) Immunogenic properties of the glial fibrillary acidic protein.Brain Research 115, 150–7.

    PubMed  Google Scholar 

  • Dahl, D. &Bignami, A. (1977) Preparation of antisera to neurofilament protein from chicken brain and human sciatic nerve.Journal of Comparative Neurology 176, 645–58.

    PubMed  Google Scholar 

  • Dahl, D., Selkoe, D. J., Pero, R. T. &Bignami, A. (1982) Immunostaining of neurofibrillary tangles in Alzheimer's senile dementia with a neurofilament antiserum.Journal of Neuroscience 2, 113–9.

    PubMed  Google Scholar 

  • Ehinger, B. &Falck, B. (1966) Concomitant adrenergic and parasympathetic fibers in the rat iris.Acta Physiologica Scandinavica 67, 201–7.

    PubMed  Google Scholar 

  • Ehinger, B. &Falck, B. (1970) Innervation of iridic melanophores.Zeitschrift für Zellforschung und mikroskopische Anatomie 105, 538–42.

    Google Scholar 

  • Falck, B. (1962) Observations on the possibilities of the cellular localization of monoamines by a fluorescence method.Acta Physiologica Scandinavica, Suppl. 197,56, 1–25.

    Google Scholar 

  • Falck, B., Hillarp, N.-Å., Thieme, G. &Torp, A. (1962) Fluorescence of catecholamines and related compounds condensed with formaldehyde.Journal of Histochemistry and Cytochemistry 10, 348–54.

    Google Scholar 

  • Gabella, G. (1974) The sphincter pupillae of the guinea-pig: structure of muscle cells, intercellular relations and density of innervation.Proceedings of the Royal Society of London Series B 186, 369–86.

    Google Scholar 

  • Hillarp, N.-Å. (1946) Structure of the synapse and the peripheral innervation apparatus of the autonomie nervous system.Acta Anatomica, Basel, Suppl. 4, 1–153.

    Google Scholar 

  • Huhtala, A. (1976) Origin of myelinated nerves in the rat iris.Experimental Eye Research 22, 259–65.

    PubMed  Google Scholar 

  • Huhtala, A. &Palkama, A. (1975) Myelinated nerves in the rat iris. An electron microscopic study.Journal of Ultrastructure Research 50, 381–2.

    Google Scholar 

  • HöKfelt, T. (1966) Electron microscopic observations on nerve terminals in the intrinsic muscles of the albino rat iris.Acta Physiologica Scandinavica 67, 255–6.

    PubMed  Google Scholar 

  • HöKfelt, T. (1967) Ultrastructural studies on adrenergic nerve terminals in the albino rat iris after pharmacological and experimental treatment.Acta Physiologica Scandinavica 69, 125–6.

    PubMed  Google Scholar 

  • Hökfelt, T. (1969) Distribution of noradrenaline storing particles in peripheral adrenergic neurons as revealed by electron microscopy.Acta Physiologica Scandinavica 76, 427–40.

    PubMed  Google Scholar 

  • Hökfelt, T. (1973) Neuronal catecholamine storage vesicles. InFrontiers in Catecholamine Research (edited byUsdin, E. andSnyder, S.), pp. 439–446. Oxford: Pergamon Press.

    Google Scholar 

  • Hökfelt, T., &Nilsson, O. (1965) The relationship between nerves and smooth muscle cells in the rat iris. II. The sphincter muscle.Zeitschrift für Zellforschung und mikroskopische Anatomie 66, 848–53.

    Google Scholar 

  • Ivens, C., Mottram, D. R., Lever, J. D., Presley, R. &Howells, G. (1973) Studies On the acetylcholinesterase(Ache)-positive and -negative autonomie axons supplying smooth muscle in the normal and 6-hydroxydopamine (6-OHDA) treated rat iris.Zeitschrift für Zellforschung und mikroskopische Anatomie 138, 211–22.

    Google Scholar 

  • Karnovsky, M. J. &Roots, L. (1964) A ‘direct-cloring’ thiocholine method for cholinesterase.Journal of Histochemistry and Cytochemistry 12, 219–21.

    PubMed  Google Scholar 

  • Krapp, J. (1962) Electronmikroskopische Untersuchungen uber die Innervation von Iris und Corpus ciliare der Hauskatze unter besonderer Berucksichtigung der Muskulatur.Zeitschrift für Zellforschung und mikroskopische Anatomie 68, 418–47.

    Google Scholar 

  • Lim, W. C. &Webber, W. A. (1975) A scanning electron-microscopic study of the posterior and anterior surface of the rat iris in pupillary dilation and constriction.Experimental Eye Research 20, 445–62.

    PubMed  Google Scholar 

  • Linder, J. E. (1978) A simple and reliable method for the silver impregnation of nerves in paraffin sections of soft and mineralized tissues.Journal of Anatomy 127, 543–51.

    PubMed  Google Scholar 

  • Malmfors, T. (1965) Studies on adrenergic nerves. The use of rat and mouse iris for direct observations on their physiology and pharmacology at cellular and subcellular levels.Acta Physiologica Scandinavica, Suppl. 248, 1–93.

    Google Scholar 

  • Miller, A., Costa, M., Furness, J. B. &Chubb, J. W. (1981) Substance P immunoreactive sensory nerves supply the rat iris and cornea.Neuroscience Letters 23, 243–9.

    PubMed  Google Scholar 

  • Nilsson, O. (1964) The relationship between nerves and smooth muscle cells in the rat iris. I. The dilator muscle.Zeitschrift für Zellforschung und mikroskopische Anatomie 64, 166–71.

    Google Scholar 

  • Nishida, S. &Sears, M. (1969a) Fine structural innervation of the dilator muscle of the iris of the albino guinea pig studied with permanganate fixation.Experimental Eye Research 8, 292–6.

    PubMed  Google Scholar 

  • Nishida, S. &Sears, M. (1969b) Dual innervation of the iris sphincter muscle of the albino guinea pig.Experimental Eye Research 8, 467–9.

    PubMed  Google Scholar 

  • Ochi, J., Konishi, M., Yoshikawa, H. &Sano, Y. (1968) Fluorescence and electron microscopic evidence for the dual innervation of the iris sphincter muscle of the rabbit.Zeitschrift für Zellforschung und mikroskopische Anatomie 91, 90–5.

    Google Scholar 

  • Olson, L., Seiger, Å., &Strömberg, I. (1983) Intraocular transplantation in rodents. A detailed account of the procedure and examples of its use in neurobiology with special reference to brain tissue grafting. InAdvances in Cellular Neurobiology (edited byFedoroff, S. andHertz, L.), Vol. 4, pp. 407–442. New York: Academic Press.

    Google Scholar 

  • Olson, L. &Ungerstedt, U. (1970) A simple high capacity freeze-drier for histochemical use.Histochemie 22, 8–19.

    PubMed  Google Scholar 

  • Raju, T. R. &Dahl, D. (1982) Immunofluorescence staining of cultured neurons: A comparative study using tetanus toxin and neurofilament antisera.Brain Research 248, 196–200.

    PubMed  Google Scholar 

  • Richardson, K. C. (1964) The fine structure of the albino rabbit iris with special reference to the identification of adrenergic and cholinergic nerves and nerve endings in its intrinsic muscles.American Journal of Anatomy 114, 173–205.

    PubMed  Google Scholar 

  • Richardson, K. C. (1966) Electron microscopic identification of autonomie nerve endings.Nature 210, 756.

    Google Scholar 

  • Roth, C. D. &Richardson, K. C. (1969) Electron microscopical studies on axonal degeneration in the rat iris following ganglionectomy.American Journal of Anatomy 124, 341–60.

    PubMed  Google Scholar 

  • Saari, M. &Johansson, G. (1974) Myelinated nerves of the rat iris.Acta Anatomica, Basel 89, 139–44.

    Google Scholar 

  • Saari, M., Kiviniemi, P., Johansson, G. &Huhtala, A. (1973) Wallerian degeneration of the myelinated nerves of rat iris after denervation of the ophthalmic division of the trigeminal nerve: An electron microscopic study.Experimental Eye Research 17, 281–7.

    PubMed  Google Scholar 

  • Schonfeld, A. R., Kress, Y., Raine, C. S. &Katzman, R. (1982) An electron microscope autoradiographic study of regenerating locus coeruleus fibers into iris tissue implants in the rat mesencephalon.Brain Research 249, 203–10.

    PubMed  Google Scholar 

  • Schultzberg, M., Hökfelt, T., Olson, L., Ålund, M., Nilsson, G., Terenius, L., Elde, R., Goldstein, M. &Said, S. (1980) Substance P, VIP, enkephalin and somatostatin immunoreactive neurons in intestinal tissue transplanted to the anterior eye chamber.Journal of the Autonomie Nervous System 1, 293–303.

    Google Scholar 

  • Seiger, Å., Dahl, D., Ayer-Lelievre, C. &Björklund, H. (1984) Appearance and distribution of neurofilament immunoreactivity in iris nerves.Journal of Comparative Neurology 223, 457–70.

    PubMed  Google Scholar 

  • Shimizu, Y., Ishimoto, I., Shiosaka, S., Kuwayama, Y., Fukuda, M., Inagaki, S., Sakanaka, M. &Tohyama, M. (1982) A direct contact of substance P-containing nerve fibers with pupillary sphincter muscles of the rat: An immunohistochemical analysis.Neuroscience Letters 33, 25–28.

    PubMed  Google Scholar 

  • Stefanini, M., Demartino, C. &Zamboni, D. (1967) Fixation of ejaculated spermatozoa for electron microscopy.Nature 216, 173–4.

    PubMed  Google Scholar 

  • Tranzer, J. P. (1973) New aspects of the localization of catecholamines in adrenergic neurons. InFrontiers in Catecholamine Research (edited byUsdin, E. andSnyder, S.), pp. 553–558. Oxford: Pergamon Press.

    Google Scholar 

  • Tranzer, J.-P. &Richards, J. G. (1976) Ultrastructural cytochemistry of biogenic amines in nervous tissue: Methodologic improvements.Journal of Histochemistry and Cytochemistry 24, 1178–93.

    PubMed  Google Scholar 

  • Tranzer, J. P. &Thoenen, H. (1968) Various types of amine-storing vesicles in peripheral adrenergic nerve terminals.Experientia 24, 484–6.

    PubMed  Google Scholar 

  • Uehara, Y. &Burnstock, G. (1972) Postsynaptic specialization of smooth muscle at close neuromuscular junctions in the guinea pig sphincter pupillae.Journal of Cell Biology 53, 849–53.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, Uppsala University, Uppsala, Sweden

    Kjell-Olof Hedlund

  2. Department of Histology, Karolinska Institutet, Stockholm, Sweden

    Christiane Ayer-Lelievre, Håkan Björklund, Lena Hultgren & Åke Seiger

Authors
  1. Kjell-Olof Hedlund
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  2. Christiane Ayer-Lelievre
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  3. Håkan Björklund
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  4. Lena Hultgren
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  5. Åke Seiger
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Hedlund, KO., Ayer-Lelievre, C., Björklund, H. et al. Ultrastructural and histochemical studies of the rat iris: identified neuronal inputs and supportive glia. J Neurocytol 13, 703–725 (1984). https://doi.org/10.1007/BF01148490

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  • DOI: https://doi.org/10.1007/BF01148490

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