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Co-localization of glutamic acid decarboxylase and vesicular GABA transporter in cytochrome oxidase patches of macaque striate cortex

  • DANIEL L. ADAMS (a1) (a2), JOHN R. ECONOMIDES (a1) and JONATHAN C. HORTON (a1)

Abstract

The patches in primary visual cortex constitute hot spots of metabolic activity, manifested by enhanced levels of cytochrome oxidase (CO) activity. They are also labeled preferentially by immunostaining for glutamic acid decarboxylase (GAD), γ-aminobutyric acid (GABA), and parvalbumin. However, calbindin shows stronger immunoreactivity outside patches. In light of this discrepancy, the distribution of the vesicular GABA transporter (VGAT) was examined in striate cortex of two normal macaques. VGAT immunoreactivity was strongest in layers 4B, 4Cα, and 5. In tangential sections, the distribution of CO, GAD, and VGAT was compared in layer 2/3. There was a close match between all three labels. This finding indicates that GABA synthesis is enriched in patches, and that inhibitory synapses are more active in patches than interpatches.

Copyright

Corresponding author

*Address correspondence to: Jonathan C. Horton MD, PhD, Beckman Vision Center, University of California, San Francisco, 10 Koret Way, San Francisco, CA 94143-0730. E-mail: hortonj@vision.ucsf.edu

References

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Adams, D.L. & Horton, J.C. (2006). Monocular cells without ocular dominance columns. Journal of Neurophysiology 96, 22532264.
Celio, M.R., Scharer, L., Morrison, J.H., Norman, A.W. & Bloom, F.E. (1986). Calbindin immunoreactivity alternates with cytochrome c-oxidase-rich zones in some layers of the primate visual cortex. Nature 323, 715717.
Chaudhry, F.A., Reimer, R.J., Bellocchio, E.E., Danbolt, N.C., Osen, K.K., Edwards, R.H. & Storm-Mathisen, J. (1998). The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. The Journal of Neuroscience 18, 97339750.
Conti, F., Minelli, A. & Melone, M. (2004). GABA transporters in the mammalian cerebral cortex: Localization, development and pathological implications. Brain Research. Brain Research Reviews 45, 196212.
DeFelipe, J., Lopez-Cruz, P.L., Benavides-Piccione, R., Bielza, C., Larranaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairen, A., Feldmeyer, D., Fishell, G., Fitzpatrick, D., Freund, T.F., Gonzalez-Burgos, G., Hestrin, S., Hill, S., Hof, P.R., Huang, J., Jones, E.G., Kawaguchi, Y., Kisvarday, Z., Kubota, Y., Lewis, D.A., Marin, O., Markram, H., McBain, C.J., Meyer, H.S., Monyer, H., Nelson, S.B., Rockland, K., Rossier, J., Rubenstein, J.L., Rudy, B., Scanziani, M., Shepherd, G.M., Sherwood, C.C., Staiger, J.F., Tamas, G., Thomson, A., Wang, Y., Yuste, R. & Ascoli, G.A. (2013). New insights into the classification and nomenclature of cortical GABAergic interneurons. Nature Reviews. Neuroscience 14, 202216.
DeYoe, E.A., Trusk, T.C. & Wong-Riley, M.T. (1995). Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey. Visual Neuroscience 12, 629639.
Ding, Y. & Casagrande, V.A. (1997). The distribution and morphology of LGN K pathway axons within the layers and CO blobs of owl monkey V1. Visual Neuroscience 14, 691704.
Duffy, K.R. & Livingstone, M.S. (2003). Distribution of non-phosphorylated neurofilament in squirrel monkey V1 is complementary to the pattern of cytochrome-oxidase blobs. Cerebral Cortex 13, 722727.
Dyck, R.H., Chaudhuri, A. & Cynader, M.S. (2003). Experience-dependent regulation of the zincergic innervation of visual cortex in adult monkeys. Cerebral Cortex 13, 10941109.
Economides, J.R., Sincich, L.C., Adams, D.L. & Horton, J.C. (2011). Orientation tuning of cytochrome oxidase patches in macaque primary visual cortex. Nature Neuroscience 14, 15741580.
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). The Journal of Neuroscience 3, 673702.
Fitzpatrick, D., Lund, J.S., Schmechel, D.E. & Towles, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. The Journal of Comparative Neurology 264, 7391.
Goto, S. & Singer, W. (1994). Laminar and columnar organization of immunoreactivity for calcineurin, a calcium- and calmodulin-regulated protein phosphatase, in monkey striate cortex. Cerebral Cortex 4, 636645.
Hendrickson, A.E., Hunt, S.P. & Wu, J.Y. (1981). Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292, 605607.
Hendrickson, A.E., Tillakaratne, N.J., Mehra, R.D., Esclapez, M., Erickson, A., Vician, L. & Tobin, A.J. (1994). Differential localization of two glutamic acid decarboxylases (GAD65 and GAD67) in adult monkey visual cortex. The Journal of Comparative Neurology 343, 566581.
Hendry, S. & Carder, R.K. (1992). Organization and plasticity of GABA neurons and receptors in monkey visual cortex. Progress in Brain Research 90, 477502.
Hendry, S.H. (1991). Delayed reduction in GABA and GAD immunoreactivity of neurons in the adult monkey dorsal lateral geniculate nucleus following monocular deprivation or enucleation. Experimental Brain Research 86, 4759.
Hendry, S.H., Huntsman, M.M., Viñuela, A., Möhler, H., de, Blas, A.L. & Jones, E.G. (1994). GABAA receptor subunit immunoreactivity in primate visual cortex: Distribution in macaques and humans and regulation by visual input in adulthood. The Journal of Neuroscience 14, 23832401.
Hendry, S.H. & Yoshioka, T. (1994). A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575577.
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 304, 199253.
Horton, J.C. & Adams, D.L. (2005). The cortical column: A structure without a function. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 837862.
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762764.
Hübener, M. & Bolz, J. (1992). Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. The Journal of Comparative Neurology 324, 6780.
Kaskan, P.M., Lu, H.D., Dillenburger, B.C., Roe, A.W. & Kaas, J.H. (2007). Intrinsic-signal optical imaging reveals cryptic ocular dominance columns in primary visual cortex of New World owl monkeys. Frontiers in Neuroscience 1, 6775.
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Sciences of the United States of America 79, 60986101.
McIntire, S.L., Reimer, R.J., Schuske, K., Edwards, R.H. & Jorgensen, E.M. (1997). Identification and characterization of the vesicular GABA transporter. Nature 389, 870876.
Nie, F. & Wong-Riley, M.T. (1996). Differential glutamatergic innervation in cytochrome oxidase-rich and -poor regions of the macaque striate cortex: Quantitative EM analysis of neurons and neuropil. The Journal of Comparative Neurology 369, 571590.
Weltzien, F., Dimarco, S., Protti, D.A., Daraio, T., Martin, P.R. & Grunert, U. (2014). Characterization of secretagogin-immunoreactive amacrine cells in marmoset retina. The Journal of Comparative Neurology 522, 435455.
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, 1128.
Wong-Riley, M.T.T. (1994). Primate visual cortex: Dynamic metabolic organization and plasticity revealed by cytochrome oxidase. In Cerebral Cortex, eds. Peters, A. & Rockland, K.S., pp. 141200. New York: Plenum Press.
Xu, X., Bosking, W.H., White, L.E., Fitzpatrick, D. & Casagrande, V.A. (2005). Functional organization of visual cortex in the prosimian bush baby revealed by optical imaging of intrinsic signals. Journal of Neurophysiology 94, 27482762.

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