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Three-dimensional microanatomy of perineuronal proteoglycan nets enveloping motor neurons in the rat spinal cord

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Journal of Neurocytology

Abstract

Summary. Spinal motor neurons possess reticular coats of extracellular matrix proteoglycans on their somata and proximal dendrites. In order to define the anatomical background of the network, spatial relationships of the perineuronal proteoglycans with synaptic boutons and astrocyte processes were analyzed in rat motor neurons by TEM after histochemical detection of the substances with cationic iron colloid, and by SEM after exposure of the cytoarchitecture with NaOH maceration. Narrow intercellular channels filled with proteoglycan were found to extend along the surface of the neurons to form a homogeneous network of a mesh size of about 1 µm. The system of perineuronal channels consisted of two parts: a primary intervaricose net which meandered among synaptic boutons on the surface of the motor neuron, and secondary subvaricose nets which irrigated interfaces between larger boutons and the neuron. No elements in the perineuronal cytoarchitecture coincided with the meshwork of proteoglycan, indicating the involvement of postsynaptic factors in the distribution of the substance. Thin astrocyte processes surrounding the neurons formed a distinct network with heterogeneous meshes corresponding to boutons of various sizes. The perineuronal glial nets extended their surface area in contact with the intervaricose nets of proteoglycan by complex cellular interdigitations. The subvaricose nets of proteoglycan compartmentalized multiple synapses on large boutons, suggesting an involvement in the division of the synapses during development.

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References

  • Arimatsu, Y., Naegele, J. R. & Barnstable, C. J. (1987) Molecular markers of neuronal subpopulations in layers 4, 5 and 6 of cat primary visual cortex. Journal of Neuroscience 7, 1250–63.

    Google Scholar 

  • Bignami, A., Asher, R. & Perides, G. (1992a) The extracellular matrix of rat spinal cord: a comparative study on the localization of hyaluronic acid, glial hyaluronate-binding protein, and chondroitin sulfate proteoglycan. Experimental Neurology 117, 90–3.

    Google Scholar 

  • Bignami, A., Asher, R., Perides, G. & Rahemtulla, F. (1992b) the extracellular matrix of cerebral gray matter: Golgi′s pericellular net and Nissl′s nervösen Grau revisited. International Journal of Developmental Neuroscience 10, 291–9.

    Google Scholar 

  • BlÑmcke, I., Eggli, P. & Celio, M. R. (1995) Relationship between astrocytic processes and ″perineuronal nets″ in rat neocortex. Glia 15, 131–40.

    Google Scholar 

  • Brauer, K., BrÑckner, G., Leibnitz, L. & Werner, L. (1984) Structural and cytochemical features of perineuronal glial nets in the rat brain. Acta Histochemica 74, 53–60.

    Google Scholar 

  • BrÑckner, G., Brauer, K., HÄrtig, W., Wolff, J. R., Rickmann, M. J., Derouiche, A., Delpech, B., Girad, N., Oertel, W. H. & Reichenbach, A. (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8, 183–200.

    Google Scholar 

  • BrÑckner, G., HÄrtig, W., Kacza, J., Seeger, J., Welt, K. & Brauer, K. (1996) Extracellular matrix organization in various regions of rat brain gray matter. Journal of Neurocytology 25, 333–46.

    Google Scholar 

  • Celio, M. R. & BlÑmcke, I. (1994) Perineuronal nets—a specialized form of extracellular matrix in the adult nervous system. Brain Research Reviews 19, 128–45.

    Google Scholar 

  • Conradi, S. (1969a) Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiologica Scandinavica Supplementum 332, 5–48.

    Google Scholar 

  • Conradi, S. (1969b) Ultrastructure and distribution of neuronal and glial elements on the surface of the proximal part of a motoneuron dendrite, as analysed by serial sections. Acta Physiologica Scandinavica Supplementum 332, 49–64.

    Google Scholar 

  • Conradi, S. & Skoglund, S. (1969) Observations on the ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the cat during postnatal development. Acta Physiologica Scandinavica Supplementum 333, 5–52.

    Google Scholar 

  • Derouiche, A. & Frotscher, M. (1991) Astroglial processes around identified glutamatergic synapses contain glutamine synthetase: evidence for transmitter degradation. Brain Research 552, 346–50.

    Google Scholar 

  • Derouiche, A., HÄrtig, W., Brauer. K. & BrÑckner, G. (1996) Spatial relationship of lectin-labelled extracellular matrix and glutamine synthetaseimmunoreactive astrocytes in rat cortical forebrain regions. Journal of Anatomy 189, 363–72.

    Google Scholar 

  • Fujita, S. C., Tada, Y., Murakami, F., Hayashi, M. & Matsumura, M. (1989) Glycosaminoglycanrelated epitopes surrounding different subsets of mammalian central neurons. Neuroscience Research 7, 117–30.

    Google Scholar 

  • Golgi, C. (1898) Sur la structure des cellules nerveuses. Archives Italiennes de Biologie 30, 60–71.

    Google Scholar 

  • Hockfield, S. & McKay, R. D. G. (1983) A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proceedings of the National Academy of Sciences USA 80, 5758–61.

    Google Scholar 

  • Kalb, R. G. & Hockfield, S. (1988) Molecular evidence for early activity-dependent development of hamster motor neurons. Journal of Neuroscience 8, 2350–60.

    Google Scholar 

  • Kalb, R. G. & Hockfield, S. (1990) Induction of a neuronal protoglycan by the NMDA receptor in the developing spinal cord. Science 250, 294–6.

    Google Scholar 

  • Lafarga, M., Berciano, M. T. & Blanco, M. (1984) The perineuronal net in the fastigial nucleus of the rat cerebellum. Anatomy and Embryology 170, 79–85.

    Google Scholar 

  • Margolis, R. U. & Margolis, R. K. (1994) Aggrecan-versican-neurocan family of proteoglycans. Methods in Enzymology 245, 105–26.

    Google Scholar 

  • Martinotti, C. (1897) Sur quelques particularités des cellules nerveuses de la moelle épinière mises en évidence avec la réaction noire de Golgi. Archives Italiennes de Biologie 27, 253–4.

    Google Scholar 

  • Murakami, T., Taguchi, T., Ohtsuka, A., Sano, K., Kaneshige, T., Owen, R. L. & Jones, A. L. (1986) A modified method of fine-granular cationic iron colloid preparation: its use in light and electron microscopic detection of anionic sites in the rat kidney glomerulus and certain other tissues. Archivum Histologicum Japonicum 49, 13–23.

    Google Scholar 

  • Murakami, T., Tsubouchi, Y., Tsubouchi, M., Ohtsuka, A., Taguchi, T. & Kikuta, A. (1993) The occurrence of rat spinal cord neurons with strongly negative-charged surface coats. Archives of Histology and Cytology 56, 501–4.

    Google Scholar 

  • Murakami, T., Ohtsuka, A. & Taguchi, T. (1994) Neurons with intensely negatively charged extracellular matrix in the human visual cortex. Archives of Histology and Cytology 57, 509–22.

    Google Scholar 

  • Murakami, T., Ohtsuka, A. & Ono, K. (1996) Neurons with perineuronal sulfated proteoglycans in the mouse brain and spinal cord: their distribution and reactions to lectin Vicia villosa agglutinin and Golgi′s silver nitrate. Archives of Histology and Cytology 59, 219–31.

    Google Scholar 

  • Naegele, J. R., Arimatsu, Y., Schwartz, P. & Barnstable, C. J. (1988) Selective staining of a subset of GABAergic neurons in cat visual cortex by monoclonal antibody VC 1.1. Journal of Neuroscience 8, 79–89.

    Google Scholar 

  • Nicholson, C. & SykovÁ, E. (1998) Extracellular space structure revealed by diffusion analysis. Trends in Neurosciences 21, 207–15.

    Google Scholar 

  • Palay, S. L. & Chan-Palay, V. (1974) Cerebellar Cortex. Cytology and Organization, pp. 311–16. Berlin, Heidelberg, New York: Springer.

    Google Scholar 

  • Schweizer, M., Streit, W. J. & MÑller C. M. (1993) Postnatal development and localization of an Nacetylgalactosamine containing glycoconjugate associated with nonpyramidal neurons in cat visual cortex. Journal of Comparative Neurology 329, 313–27.

    Google Scholar 

  • Takahashi-Iwanaga, H. (1992) Reticular endings of Purkinje cell axons in the rat cerebellar nuclei: scanning electron microscopic observation of the pericellular plexus of Cajal. Archives of Histology and Cytology 55, 307–14.

    Google Scholar 

  • Takahashi-Iwanaga, H. & Fujita, T. (1986) Application of an NaOH maceration method to a scanning electron microscopic observation of Ito cells in the rat liver. Archivum Hisotologicum Japonicum 49, 349–57.

    Google Scholar 

  • Takahashi-Iwanaga, H. & Fujita, T. (1994) Scanning electron microscopic observation of the rat cerebellar cortex. Acta Medica et Biologica 42, 25–9.

    Google Scholar 

  • Watanabe, E., Fujita, S. C., Murakami, F., Hayashi, M. & Matsumura, M. (1989) A monoclonal antibody identifies a novel epitope surrounding a subpopulation of the mammalian central neurons. Neuroscience 29, 645–57.

    Google Scholar 

  • Zaremba, S., Guimaraes, A., Kalb, R. G. & Hockfield, S. (1989) Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 2, 1207–19.

    Google Scholar 

  • Zaremba, S., Naegele, J. R., Barnstable, C. J. & Hockfield, S. (1990) Neuronal subsets express multiple high-molecular-weight cell-surface glycoconjugates defined by monoclonal antibodies Cat-301 and VC 1.1. Journal of Neuroscience 10, 2985–95.

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Hokkaido University Graduate School of Medicine, Kita-15, Nishi 7, Sapporo, 060-8638, Japan

    HIROMI Takahashi-IWANAGA & KAZUHIRO Abe

  2. Department of Anatomy, Okayama University School of Medicine, Shikadacho 2-5-1, Okayama, 700-8558, Japan

    TAKURO Murakami

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  1. HIROMI Takahashi-IWANAGA
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  2. TAKURO Murakami
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  3. KAZUHIRO Abe
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Takahashi-IWANAGA, H., Murakami, T. & Abe, K. Three-dimensional microanatomy of perineuronal proteoglycan nets enveloping motor neurons in the rat spinal cord. J Neurocytol 27, 817–827 (1998). https://doi.org/10.1023/A:1006955414939

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