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The Lectin Vicia Villosa Labels a Distinct Subset of GABAergic Cells in Macaque Visual Cortex

Published online by Cambridge University Press:  02 June 2009

K. A. Mulligan ,
J. F. M. Van Brederode  and
A. E. Hendrickson
K. A. Mulligan
Affiliation:
Department of Biological Structure, University of Washington School of Medicine, Seattle
J. F. M. Van Brederode
Affiliation:
Department of Biological Structure, University of Washington School of Medicine, Seattle
A. E. Hendrickson
Affiliation:
Department of Biological Structure, University of Washington School of Medicine, Seattle Departments of Biological Structure and Ophthalmology, University of Washington School of Medicine, Seattle
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Abstract

The morphology and distribution of neurons labeled specifically by the lectin, Vicia villosa (VVA), were examined in striate cortex of adult macaque monkeys. Following incubation with VVA conjugated to histochemical markers, fine punctate reaction product appears to cover the surface of the soma and proximal dendrites of a population of cortical neurons. Although a small number of VVA-labeled cells are located in layers 2, 3A, 5, and 6, approximately 75% are located in a strip of cortex overlying layers 3B through 4Ca. Layers 1 and 4Cβ are virtually devoid of labeled cells. The morphology of labeled cells varies throughout the layers. In the supragranular layers, the labeled cells generally display a round or multipolar soma with a small number of radially disposed dendrites. In deeper layers, labeled cells are multipolar or horizontal, and their proximal dendrites are often more densely labeled. There is no clear correlation between the distribution of labeled cells and the pattern of cytochrome oxidase staining in supragranular layers.

Double labeling of single sections for VVA and for GABA (gamma-aminobutyric acid) immunoreactivity revealed that most VVA-labeled cells are also immunoreactive for GABA. The double-labeled cells comprise approximately 30% of all GABA immunoreactive cells. Soma size analysis of double-labeled cells shows that medium-to-large GABA cells in each layer are labeled by VVA. The soma size, laminar distribution, and morphology of the VVA-labeled GABA cells suggest that they include the large basket cells originally observed in Golgi preparations.

Keywords

LectinVisual cortexBasket cells
Type
Research Articles
Information
Visual Neuroscience , Volume 2 , Issue 1 , January 1989 , pp. 63 - 72
Copyright
Copyright © Cambridge University Press 1989

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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, 1250–1263.CrossRefGoogle Scholar
Bowker, R.M., Westlund, K.N., Sullivan, M.C. & Coulter, J.D. (1982). A combined retrograde transport and immunocytochemical staining method for demonstrating the origins of serotonergic projections. Journal of Histochemistry and Cytochemistry 8, 805–810.CrossRefGoogle Scholar
Curcio, C.A. & Sloan, K.R. Jr., (1986). Computer-assisted morphometry using video-mixed microscopic images and computer graphics. Anatomical Record 214, 329–337.CrossRefGoogle ScholarPubMed
DeFelipe, J., Hendry, S.H.C. & Jones, E.G. (1986). A correlative electron-microscopic study of basket cells and large GABAergic neurons in the monkey sensory-motor cortex. Neuroscience 17, 991–1009.CrossRefGoogle ScholarPubMed
Delpech, A., Girard, N. & Delpech, B. (1982). Localization of hyaluronectin in the nervous system. Brain Research 245, 251–257.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S., Schmechel, D.E. & Towles, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Hunt, S.P. & Wu, J.Y. (1981). Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292, 605–607.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Houser, C.R., Jones, E.G. & Vaughn, J.E. (1983). Synaptic organization of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. Journal of Neurocytology 12, 639–660.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Jones, E.G. (1981). Sizes and distribution of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex. Journal of Neuroscience 1, 390–408.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G., DeFelipe, J., Schmechel, D., Brandon, C. & Emson, P.C. (1984 a). Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. Proceedings of the National Academy of Sciences of the U.S.A. 81, 6526–6530.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G. & Emson, P.C. (1984 b). Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. Journal of Neuroscience 4, 2497–2517.CrossRefGoogle ScholarPubMed
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, 518–542.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Schwark, H.D., Jones, E.G. & Yan, J. (1987). Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. Journal of Neuroscience 7, 1503–1519.CrossRefGoogle ScholarPubMed
Hockfield, S., McKay, R.D.G., Hendry, S.H.C. & Jones, E.G. (1983). A surface antigen that identifies ocular dominance columns in the visual cortex and laminar features of the lateral geniculate nucleus. Cold Spring Harbor Symposium on Quantitative Biology 48, 877–889.CrossRefGoogle ScholarPubMed
Houser, C.R., Hendry, S.H.C., Jones, E.G. & Vaughn, J.E. (1983). Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. Journal of Neurocytology 12, 617–628.CrossRefGoogle ScholarPubMed
Houser, C.R., Vaughn, J.E., Hendry, S.H.C., Jones, E.G. & Peters, A. (1984). GABA neurons in the cerebral cortex. In Cerebral Cortex, Vol. 2: ed. Jones, E.G. & Peters, A., pp. 63–89. New York: Plenum Press.CrossRefGoogle Scholar
Humphrey, A.L. & Hendrickson, A.E. (1983). Background and stimulus-induced patterns of high metabolic activity in the visual cortex of the squirrel and macaque monkey. Journal of Neuroscience 3, 345–358.CrossRefGoogle ScholarPubMed
Jones, E.G. (1975). Varieties and distribution of nonpyramidal cells in the somatic sensory cortex of the squirrel monkey. Journal of Comparative Neurology 160, 205–268.CrossRefGoogle ScholarPubMed
Jones, E.G. & Hendry, S.H.C. (1984). Basket cells. In Cerebral Cortex, Vol. 1, 1: ed. Peters, A. & Jones, E.G., pp. 309–336. New York: Plenum Press.CrossRefGoogle Scholar
Jones, E.G. & Hendry, S.H.C. (1986). Co-localization of GABA and neuropeptides in neocortical neurons. Trends in Neurosciences 9, 71–76.CrossRefGoogle Scholar
Kisvarday, Z.F., Martin, K.A.C., Friedlander, M.J. & Somogyi, P. (1987). Evidence for interlaminar inhibitory circuits in the striate cortex of the cat. Journal of Comparative Neurology 260, 1–19.CrossRefGoogle ScholarPubMed
Kuljis, R.O. & Rakic, P. (1987). NPY neurons are situated predominantly outside CO-positive blobs in layers 2–3 of macaque striate cortex. Society for Neuroscience Abstracts 13, 359.Google Scholar
Kushner, P.D. (1984). A library of monoclonal antibodies to Torpedo cholinergic synaptosomes. Journal of Neurochemistry 43, 775–786.CrossRefGoogle ScholarPubMed
McKay, R.D.G. & Hockfield, S.J. (1982). Monoclonal antibodies distinguish antigenically discrete neuronal types in the vertebrate central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 79, 6747–6751.CrossRefGoogle ScholarPubMed
Mehra, R. & Hendrickson, A. (1987). Developmental studies of substance P and neuropeptide Y neurons in monkey visual cortex. Society for Neuroscience Abstracts 13, 358.Google Scholar
Mehra, R., Hendrickson, A.E. & Streit, P. (1989). Distribution of the neuropeptides substance P and neuropeptide Y in the macaque visual cortex during prenatal and postnatal development. Submitted.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 VC1.1. Journal of Neuroscience 8, 79–89.CrossRefGoogle ScholarPubMed
Nakagawa, F., Schulte, B.A. & Spicer, S.S. (1986 a). Selective cytochemical demonstration of glycoconjugate-containing terminal N-acetylgalactosamine on some brain neurons. Journal of Comparative Neurology 243, 280–290.CrossRefGoogle ScholarPubMed
Nakagawa, F., Schulte, B.A., Wu, J.-Y. & Spicer, S.S. (1986 b). GABAergic neurons of rodent brain correspond partially with those staining for glycoconjugate with terminal N-acetylgalactosamine. Journal of Neurocytology 15, 389–396.CrossRefGoogle ScholarPubMed
Rockel, A.J., Hiorns, R.W. & Powell, T.P.S. (1980). The basic uniformity in structure of the neocortex. Brain 103, 221–244.CrossRefGoogle ScholarPubMed
Somogyi, P. (1986). Seven distinct types of GABA-immunoreactive neuron in the visual cortex of cat. Society for Neuroscience Abstracts 12, 583.Google Scholar
Somogyi, P., Freund, T.F. & Kisvarday, Z.F. (1984 a). Different types of 3H-GABA accumulating neurons in the visual cortex of the rat. Characterization by combined autoradiography and Golgi impregnation. Experimental Brain Research 54, 45–56.CrossRefGoogle ScholarPubMed
Somogyi, P., Hodgson, A.J., Smith, A.D., Nunzi, M.G., Gorio, A. & Wu, J.-Y. (1984 b). Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatinor cholecystokinin-immunoreactive material. Journal of Neuroscience 4, 2590–2603.CrossRefGoogle ScholarPubMed
Somogyi, P. & Soltesz, I. (1986). Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19, 1051–1065.CrossRefGoogle ScholarPubMed
Tollefsen, S.E. & Kornfeld, R. (1983 a). Isolation and characterization of lectins from Vicia villosa. Two distinct carbohydrate binding activities are present in seed extracts. Journal of Biological Chemistry 258, 5165–5171.CrossRefGoogle ScholarPubMed
Tollefsen, S.E. & Kornfeld, R. (1983 b). The B4 lectin from Vicia villosa interacts with N-acetylgalactosamine residues a-linked to serine or threonine residues in cell surface glycoproteins. Journal of Biological Chemistry 258, 5172–5176.CrossRefGoogle ScholarPubMed
Wong—Riley, M.T.T. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed