Skip to main content
SpringerLink
Log in

VVA-labelled cells in monkey visual cortex are double-labelled by a polyclonal antibody to a cell surface epitope

  • Published:
Journal of Neurocytology

Summary

The staining patterns produced by the lectinVicia villosa and by a commercially available polyclonal antibody generated to substance P were analysed and compared in monkey visual cortex at the light and electron microscopic levels.Vicia villosa lectin labels the cell surface of a subpopulation of cortical cells, producing a meshlike pattern over the soma and proximal dendrites. The polyclonal antibody labels three distinct elements in the cortex: a pericellular epitope present on a subpopulation of non-pyramidal cells, and putative intracellular sites in a type of small pyramidal cell located at the layer 5/6 border, and in a small number of non-pyramidal cells in the underlying white matter. Because of the similarity of the appearance of theVicia villosa lectin labelling and the pericellular labelling produced by the polyclonal antibody, further experiments were conducted to determine the relationship between the cell surface sites recognized by these markers. Double-labelling experiments show that both sites are present on the same population of cells, and at the ultrastructural level both markers appear to outline the intersynaptic cell membrane, sometimes extending around presynaptic elements. However, preadsorption experiments indicate that the markers recognize different sites on the cell membrane. Preadsorption experiments also show that the pericellular epitope recognized by the polyclonal antibody is unlikely to be substance P, but it may be structurally similar to keyhole limpet haemocyanin. Comparison of cortical and subcortical staining patterns produced with the polyclonal antibody and with a commonly used monoclonal antibody to substance P reveal that one of the putative intracellular epitopes recognized by the polyclonal antibody is likely to be substance P.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

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.

    PubMed  Google Scholar 

  • Beach, T. G. &McGeer, E. G. (1983) Neocortical substance P neurons in the baboon: an immunohistochemical finding.Neuroscience Letters 41, 265–70.

    PubMed  Google Scholar 

  • Burkhalter, A. &Charles, V. (1990) Organization of local axon collaterals of efferent projection neurons in rat visual cortex.Journal of Comparative Neurology 302, 920–34.

    PubMed  Google Scholar 

  • Campbell, M. J. &Morrison, J. H. (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex.Journal of Comparative Neurology 28, 191–205.

    Google Scholar 

  • Cuello, A. C. &Kanazawa, I. (1978) The distribution of substance P immunoreactive fibers in the rat central nervous system.Journal of Comparative Neurology 178, 129–56.

    PubMed  Google Scholar 

  • Defelipe, J., Hendry, S. H. C., Hashikawa, T., Molinari, M. &Jones, E. G. (1990) A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons.Neuroscience 37, 655–73.

    PubMed  Google Scholar 

  • Demeulemeester, H., Vandersande, F., Orban, G. A., Brandon, C. &Vanderhaeghen, J. J. (1988) Heterogeneity of GABAergic cells in cat visual cortex.Journal of Neuroscience 8, 988–1000.

    PubMed  Google Scholar 

  • Demeulemeester, H., Arckens, L., Vandersande, F., Orban, G. A., Heizmann, C. W. &Pochet, R. (1991) Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex.Experimental Brain Research 84, 538–44.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Hallman, L. E., Schofield, B. R. &Lin, C. -S. (1988) Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat.Journal of Comparative Neurology 272, 149–60.

    PubMed  Google Scholar 

  • Hendry, S. H. C., Jones, E. G. &Emson, P. C. (1984) Morphology, distribution and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey cerebral cortex.Journal of Neuroscience 4, 2497–517.

    PubMed  Google Scholar 

  • Hendry, S. H. C., Jones, E. G., Hockfield, S. &McKay, R. D. G. (1988) Neuronal populations stained with the monoclonal antibody Cat-301 in the mammalian cerebral cortex and thalamus.Journal of Neuroscience 8, 518–42.

    PubMed  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 

  • Houser, C. R., Vaughn, J. E., Hendry, S. H. C., Jones, E. G. &Peters, A. (1984) GABA neurons in the cerebral cortex. InFunctional Properties of Cortical Cells, Vol. 2,Cerebral Cortex (edited byJones, E. G. &Peters, A.) pp. 63–89. New York: Plenum.

    Google Scholar 

  • Hsu, S. M., Raine, L. &Fanger, H. (1981) Use of avidinbiotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures.Journal of Histochemistry and Cytochemistry 29, 577–80.

    PubMed  Google Scholar 

  • Hübener, M. &Bolz, J. (1988) Morphology of identified projection neurons in layer 5 of rat visual cortex.Neuroscience Letters 94, 76–81.

    PubMed  Google Scholar 

  • Hübener, M., Schwartz, C. &Bolz, J. (1990) Morphological types of projection neurons in layer 5 of cat visual cortex.Journal of Comparative Neurology 301, 655–74.

    PubMed  Google Scholar 

  • Jones, E. G., Defelipe, J., Hendry, S. H. C., &Maggio, J. E. (1988) A study of tachykinin-immunoreactive neurons in monkey visual cortex.Journal of Neuroscience 8, 1206–24.

    PubMed  Google Scholar 

  • Kennedy, H. &Dehay, C. (1988) Functional implications of the anatomical organization of the callosal projections of visual areas V1 and V2 in the macaque monkey.Behavioural Brain Research 29, 225–36.

    PubMed  Google Scholar 

  • Kosaka, T., &Heizmann, C. W. (1989) Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine.Brain Research 483, 158–63.

    PubMed  Google Scholar 

  • Kosaka, T., Heizmann, C. W. &Barnstable, C. J. (1989) Monoclonal antibody VC1.1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex.Experimental Brain Research 78, 43–50.

    Google Scholar 

  • Kosaka, T., Isogai, K., Barnstable, C. J. &Heizmann, C. W. (1990) Monoclonal antibody HNK-1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex.Experimental Brain Research 82, 566–74.

    Google Scholar 

  • Lund, J. S., Lund, R. D., Hendrickson, A. E., Bunt, A. H. &Fuchs, A. F. (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase.Journal of Comparative Neurology 164, 287–304.

    Google Scholar 

  • McKay, R. D. G. &Hockfield, S. (1982) Monoclonal antibodies distinguish antigenically discrete neuronal types in the vertebrate central nervous system.Proceedings of the National Academy of Sciences (USA) 79, 6747–51.

    Google Scholar 

  • Mehra, R. &Hendrickson, A. E. (1987) Developmental studies of substance P and neuropeptide Y in monkey visual cortex.Society for Neuroscience Abstracts 13, 358.

    Google Scholar 

  • Mulligan, K. A. &Hendrickson, A. E. (1989) The lectin VVA labels a morphologically heterogeneous subpopulation of GABA neurons in the monkey striate cortex.Society for Neuroscience Abstracts 15, 1397.

    Google Scholar 

  • Mulligan, K. A., Van Brederode, J. F. M. &Hendrickson, A. E. (1989) The lectinVicia villosa labels a distinct subset of GABA cells in macaque visual cortex.Visual Neuroscience 2, 63–72.

    PubMed  Google Scholar 

  • Naegele, J. R. &Barnstable, C. J. (1989) Molecular determinants of GABAergic local circuit neurons in the visual cortex.Trends in Neuroscience 12, 28–34.

    Google Scholar 

  • Naegele, J. R. &Katz, L. C. (1990) Cell surface molecules containing N-acetylgalactosamine are associated with basket cells and neurogliaform cells in cat visual cortex.Journal of Neuroscience 10, 540–57.

    Google Scholar 

  • Naegele, J. R., Katz, L. C. &Barnstable, C. J. (1987) Morphologically distinct subsets of GABAergic neurons in cat area 17 have unique patterns of glycosylated molecules on their surfaces.Society for Neuroscience Abstracts 13, 359.

    Google Scholar 

  • Naegele, J. R., Arimatsu, Y., Schwartz, P. &Barn-Stable, C. J. (1988) Selective staining of a subset of GABAergic neurons in cat visual cortex by monoclonal antibody VC1.1.Journal of Neuroscience 8, 79–89.

    Google Scholar 

  • Nakagawa, F., Schulte, B. A., Wu, J. -Y. &Spicer, S. (1986) GABAergic neurons of rodent brain correspond partially with those staining for glycoconjugate with terminal N-acetylgalactosamine.Journal of Neurocytology 15, 389–96.

    Google Scholar 

  • Shatz, C. J. (1977) Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats.Journal of Comparative Neurology 172, 497–518.

    Google Scholar 

  • Shinoda, K., Yagi, H., Fujita, H., Osawa, Y. &Shio-Tani, Y. (1989) Screening of aromatase-containing neurons in rat forebrain: an immunohistochemical study with antibody against human placental antigen K-P2 (hPAX-P2).Journal of Comparative Neurology 290, 502–15.

    PubMed  Google Scholar 

  • Somogyi, P., Freund, T. F. &Kisvarday, Z. F. (1984) Different types of3H-GABA accumulating neurons in the visual cortex of the rat. Characterization by combined autoradiography and Golgi impregnation.Experimental Brain Research 54, 45–56.

    Google Scholar 

  • Stephenson, D. T. &Kushner, P. D. (1988) An atlas of a rare neuronal surface antigen in the rat central nervous system.Journal of Neuroscience 8, 3035–56.

    PubMed  Google Scholar 

  • Swadlow, H. A. (1983) Efferent systems of primary visual cortex: a review of structure and function.Brain Research Reviews 6, 1–24.

    Google Scholar 

  • Tigges, J., Tigges, M., Anschel, S., Cross, N. A., Letbetter, W. D. &McBride, R. L. (1981) Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19 and MT in squirrel monkey (Saimiri).Journal of Comparative Neurology 202, 539–60.

    PubMed  Google Scholar 

  • Tollefsen, S. E. &Kornfeld, R. (1983) The B4 lectin fromVicia villosa seeds interacts with N-acetylgalactosamine residues α-linked to serine or threonine residues in cell surface glycoproteins.Journal of Biological Chemistry 258, 5172–6.

    PubMed  Google Scholar 

  • Tsumoto, T., Sato, H. &Sobue, K. (1988) Immunohistochemical localization of a membrane-associated, 4.1-like protein in the rat visual cortex during postnatal development.Journal of Comparative Neurology 271, 30–43.

    PubMed  Google Scholar 

  • Van Brederode, J. F. M., Mulligan, K. A. &Hendrickson, A. E. (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex.Journal of Comparative Neurology 298, 1–22.

    PubMed  Google Scholar 

  • Van Essen, D., Newsome, W. T. &Bixby, J. L. (1982) The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey.Journal of Neuroscience 2, 265–83.

    PubMed  Google Scholar 

  • Wahle, P. &Meyer, G. (1989) Early postnatal development of vasoactive intestinal polypeptide- and peptide histidine isoleucine-immunoreactive structures in the cat visual cortex.Journal of Comparative Neurology 282, 215–48.

    PubMed  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.

    PubMed  Google Scholar 

  • Yamamoto, M., Marshall, P., Hemmendinger, L. M., Boyer, A. B. &Caviness, V. S. Jr (1988) Distribution of glucuronic acid- and sulfate-containing glycoproteins in the central nervous system of the adult mouse.Neuroscience Research 5, 273–98.

    PubMed  Google Scholar 

  • Zaremba, S., Naegele, J. R., Barnstable, C. J. &Hock-Field, S. (1990) Neuronal subsets express multiple high-molecular-weight cell-surface glycoconjugates defined by monoclonal antibodies Cat-301 and VC1.1.Journal of Neuroscience 10, 2985–95.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Structure, University of Washington, 98195, Seattle, Washington, USA

    K. A. Mulligan, J. F. M. Van Brederode & A. E. Hendrickson

  2. Department of Ophthalmology, University of Washington, 98195, Seattle, Washington, USA

    A. E. Hendrickson

  3. Department of Anatomy, All India Institute of Medical Sciences, New Delhi, India

    R. Mehra

Authors
  1. K. A. Mulligan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. F. M. Van Brederode
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Mehra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. E. Hendrickson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mulligan, K.A., Van Brederode, J.F.M., Mehra, R. et al. VVA-labelled cells in monkey visual cortex are double-labelled by a polyclonal antibody to a cell surface epitope. J Neurocytol 21, 244–259 (1992). https://doi.org/10.1007/BF01224759

Download citation

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01224759

Keywords

Search

Navigation