Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T15:55:12.018Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  20 October 2015

DANIEL L. ADAMS ,
JOHN R. ECONOMIDES  and
JONATHAN C. HORTON
DANIEL L. ADAMS
Affiliation:
Beckman Vision Center, University of California, San Francisco, California 94143 Center for Mind/Brain Sciences, The University of Trento, Trento, Italy
JOHN R. ECONOMIDES
Affiliation:
Beckman Vision Center, University of California, San Francisco, California 94143
JONATHAN C. HORTON*
Affiliation:
Beckman Vision Center, University of California, San Francisco, California 94143
*
*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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Cytochrome oxidaseInhibitionOcular dominance columnGABAMacaquePrimary visual cortexV1Blob
Type
Brief Communication
Information
Visual Neuroscience , Volume 32 , 2015 , E026
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, D.L. & Horton, J.C. (2006). Monocular cells without ocular dominance columns. Journal of Neurophysiology 96, 2253–2264.CrossRefGoogle ScholarPubMed
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, 715–717.CrossRefGoogle ScholarPubMed
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, 9733–9750.CrossRefGoogle ScholarPubMed
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, 196–212.CrossRefGoogle ScholarPubMed
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, 202–216.CrossRefGoogle ScholarPubMed
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, 629–639.CrossRefGoogle ScholarPubMed
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, 691–704.CrossRefGoogle ScholarPubMed
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, 722–727.CrossRefGoogle Scholar
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, 1094–1109.CrossRefGoogle ScholarPubMed
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, 1574–1580.CrossRefGoogle ScholarPubMed
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, 673–702.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. The Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
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, 636–645.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
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, 566–581.CrossRefGoogle ScholarPubMed
Hendry, S. & Carder, R.K. (1992). Organization and plasticity of GABA neurons and receptors in monkey visual cortex. Progress in Brain Research 90, 477–502.CrossRefGoogle ScholarPubMed
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, 47–59.CrossRefGoogle ScholarPubMed
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, 2383–2401.CrossRefGoogle ScholarPubMed
Hendry, S.H. & Yoshioka, T. (1994). A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577.CrossRefGoogle ScholarPubMed
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, 199–253.Google ScholarPubMed
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, 837–862.CrossRefGoogle ScholarPubMed
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.CrossRefGoogle ScholarPubMed
Hübener, M. & Bolz, J. (1992). Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. The Journal of Comparative Neurology 324, 67–80.CrossRefGoogle ScholarPubMed
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, 67–75.CrossRefGoogle ScholarPubMed
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, 6098–6101.CrossRefGoogle ScholarPubMed
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, 870–876.CrossRefGoogle ScholarPubMed
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, 571–590.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
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, 435–455.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
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. 141–200. New York: Plenum Press.Google Scholar
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, 2748–2762.CrossRefGoogle ScholarPubMed