Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-23T16:24:03.815Z Has data issue: false hasContentIssue false
  • English
  • Français

Neuronal organization and plasticity in adult monkey visual cortex: Immunoreactivity for microtubule-associated protein 2

Published online by Cambridge University Press:  02 June 2009

Stewart H. C. Hendry  and
Monica A. Bhandari
Stewart H. C. Hendry
Affiliation:
Department of Anatomy and Neurobiology, University of California, Irvine
Monica A. Bhandari
Affiliation:
Department of Anatomy and Neurobiology, University of California, Irvine
Get access Rights & Permissions [Opens in a new window]

Abstract

Immunocytochemical staining for microtubule-associated protein 2 (MAP 2) was used to examine the morphology of neurons, the organization of neuronal groups, and the neurochemical plasticity of cells in adult monkey area 17. MAP 2-immunostained neurons are present through the depth of area 17 but are most intensely immunoreactive in layers IVB and VI. From layer IVB, separate groups of MAP 2-positive cells invade layers 1VA and IVCα. Clusters of cells protrude upward from superficial layer IVB and occupy the central core regions of the cytochrome oxidase (CO)-stained honeycomb in layer IVA, while large neurons typical of layer IVB are distributed in irregular clusters in the subjacent layer IVCa. The somata in the layer IVA honeycomb cores give off immunostained dendrites which remain largely within the core regions. Patches of MAP 2-positive neurons are also present in layers II and III, where they coincide with the CO-stained puffs.

Intravitreal injections of tetrodotoxin (TTX) into one eye of adult monkeys produce stripes of alternating light and dark MAP 2 immunostaining in layer IVC. Stripes of light immunostaining coincide with stripes of light CO staining, and correspond to reduced MAP 2 immunoreactivity within cortical neurons dominated by the TTX-injected eye. In layers II and III, the MAP 2 immunostaining of patches overlying the injected-eye columns is similarly reduced. No change occurs in the MAP 2 immunostaining of layer IVA.

These data suggest that the anatomical and physiological heterogeneity of layers IVA and IVCα arises from the periodic invasion of neurons characteristic of layer IVB, that the neurons in layer IVA have dendrites confined to thalamocortical-recipient or nonrecipient zones and that the expression of MAP 2 changes in adult cortical neurons following the loss of retinal input.

Keywords

DendritesCytoskeletonStriatecortexPyramidal cells
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 5 , November 1992 , pp. 445 - 459
Copyright
Copyright © Cambridge University Press 1992

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

Aoki, C. & Siekivitz, P. (1985). Ontogenetic changes in the cyclic adenosine 3′,5′-monophosphate-stimulatable phosphorylation of cat visual cortex proteins, particularly of microtubule-associated protein 2 (MAP 2): Effects of normal and dark rearing and of the exposure to light. Journal of Neuroscience 5, 2465–2483.CrossRefGoogle ScholarPubMed
Bennett, M.K., Erondu, N.E. & Kennedy, M.B. (1983). Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain. Journal of Biological Chemistry 258, 12735–12744.CrossRefGoogle ScholarPubMed
Benson, D.L., Isackson, P.J., Gall, C.M. & Jones, E.G. (1991). Differential effects of monocular deprivation of glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase gene expression in adult monkey visual cortex. Journal of Neuroscience 11, 31–47.CrossRefGoogle ScholarPubMed
Bernhardt, R. & Matus, A. (1984). Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: A difference between dendritic and axonal cytoskeleton. Journal of Comparative Neurology 226, 203–221.CrossRefGoogle Scholar
Blasdel, G.G. & Fitzpatrick, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4, 880–895.CrossRefGoogle ScholarPubMed
Bloom, G. & Vallee, R. (1983). Association of microtubule-associated protein 2 (MAP2) with microtubules and intermediate filaments in cultured brain cells. Journal of Cell Biology 96, 1523–1531.CrossRefGoogle Scholar
Boothe, R.G., Greenough, W.T., Lund, J.S. & Wrege, K. (1979). A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemistrena monkeys. Journal of Comparative Neurology 186, 473–490.CrossRefGoogle ScholarPubMed
Born, R.T. & Tootell, R.B.H. (1991). Single-unit and 2-deoxyglucose studies of side inhibition in macaque striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 88, 7071–7075.CrossRefGoogle ScholarPubMed
Campbell, M.J. & Morrison, J.H. (1989). Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in human and monkey neocortex. Journal of Comparative Neurology 282, 191–205.CrossRefGoogle ScholarPubMed
Campbell, M.J., Lewis, D.A., Benoit, R. & Morrison, J.H. (1987). Regional heterogeneity in the distribution of somatostatin-28- and somatostatin-28 (1–12) immunoreactive profiles in monkey neocortex. Journal of Neuroscience 7, 1133–1144.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
Coleman, P.D. & Riesen, A.H. (1968). Environmental effects on cortical dendritic fields. 1. Rearing in the dark. Journal of Anatomy (London) 102, 363–374.Google Scholar
Cragg, B.G. (1967). Changes in visual cortex on first exposure of rats to light. Nature 215, 251–253.CrossRefGoogle ScholarPubMed
Cronly-Dillon, J. & Nona, S.N. (1988). Changes in cytoskeletal elements during postnatal development of cerebral cortex. In Cerebral Cortex, Volume 7: Development and Maturation of Cerebral Cortex, ed. Jones, E.G. & Peters, A., pp. 273–308. New York: Plenum Press.CrossRefGoogle Scholar
Decamilli, P., Miller, P.E., Navone, F., Theurkauf, W.E. & Vallee, R.B. (1984). Distribution of microtubule-associated protein 2 in the nervous system of the rat studied by immunofluorescence. Neuroscience 11, 817–846.Google Scholar
Deyoe, E.A., Hockfield, S., Garren, H. & Van Essen, D.C. (1990). Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey. Visual Neuroscience 5, 67–81.CrossRefGoogle ScholarPubMed
Fifkova, E. & Morales, M. (1989). Calcium-regulated contractile and cytoskeletal proteins in dendritic spines may control synaptic plasticity. Annals of the New York Academy of Science 568, 131–137.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 (Samiri sciureus). Journal of Neuroscience 3, 673–702.CrossRefGoogle Scholar
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex: Afferent and efferent connections of lamina 4C. Journal of Neuroscience 5, 3329–3349.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S., Schmechel, D. & Towles, A.D. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Graybiel, A.M. & Ragsdale, C.W. Jr (1982). Pseudocholinesterase staining in the primary visual pathway of the macaque monkey. Nature 299, 439–442.CrossRefGoogle ScholarPubMed
Hawken, M.J. & Parker, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys. Experimental Brain Research 54, 367–372.CrossRefGoogle ScholarPubMed
Heimann, R., Shelanski, M.L. & Liem, R.K.H. (1985). Microtubule-associated proteins bind specifically to the 70-kDa neurofilament protein. Journal of Cell Biology 260, 12160–12166.Google Scholar
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between dorsal lateral geniculate nucleus and visual cortex in Old and New World primates. Journal of Comparative Neurology 182, 123–136.CrossRefGoogle Scholar
Hendrickson, A.E. (1982). The orthograde axoplasmic transport auto-radiographic technique and its implications for additional neuroanatomical analysis of the striate cortex. In Cytochemical Methods in Neuroanatomy, ed. Palay, S. & Chan-Palay, V., pp. 1–16. New York: Alan Liss, Inc.Google Scholar
Hendrickson, A.E. (1985). Dots, stripes and columns in monkey visual cortex. Trends in Neuroscience 8, 406–410.CrossRefGoogle Scholar
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. & Carder, R. (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.C. & Jones, E.G. (1986). Reduction in number of GABA immunostained neurons in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Jones, E.G. (1988). Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron 1, 701–712.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Kennedy, M.B. (1986). Immunoreactivity for a calmodulin-dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1536–1540.CrossRefGoogle ScholarPubMed
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 neocortex. Journal of Neuroscience 4, 2497–2517.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, 1503–1520.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G. & Burstein, N. (1988 a). Activity-dependent regulation of tachykinin-like immunoreactivity in neurons of the monkey primary visual cortex. Journal of Neuroscience 8, 1225–1238.CrossRefGoogle Scholar
Hendry, S.H.C., Jones, E.G., Hockfield, S. & Mckay, R.D.G. (1988 b). 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., Fuchs, J., De Blas, A.L. & Jones, E.G. (1990). Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. Journal of Neuroscience 10, 2438–2450.CrossRefGoogle ScholarPubMed
Herzoo, W. & Weber, K. (1978). Fractionation of brain microtubule-associated proteins which stimulate tubulin polymerization in vitro. European Journal of Biochemistry 92, 1–8.CrossRefGoogle Scholar
Hevner, R.F. & Wong-Riley, M.T.T. (1990). Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. Journal of Neuroscience 10, 1331–1340.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
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215–243.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculocortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1977). Functional architecture of macaque monkey visual cortex. Proceedings of the Royal Society B (London) 198, 1–59.Google ScholarPubMed
Hubener, M. & Bolz, J. (1991). Cell morphology and blob pattern in monkey striate cortex. Society for Neuroscience Abstracts 17, 117.Google Scholar
Humphrey, A.L. & Hendrickson, A.E. (1983). Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey. Journal of Neuroscience 3, 345–358.CrossRefGoogle ScholarPubMed
Itaya, S.K., Itaya, P.W. & Van Hoesen, G.W. (1984). Intracortical termination of the retino-geniculo-striate pathway studied with transsynaptic tracer (wheat germ agglutinin-horseradish peroxidase) and cytochrome oxidase staining in the macaque monkey. Brain Research 304, 303–310.CrossRefGoogle ScholarPubMed
Izant, J.G. & Mcintosh, J.R. (1980). Microtubule-associated proteins: A monoclonal antibody of MAP2 binds to differentiated neurons. Proceedings of the National Academy of Sciences of the U.S.A. 77, 4741–4745.CrossRefGoogle ScholarPubMed
Jameson, L. & Caplow, M. (1981). Modification of microtubule steady-state dynamics by phosphorylation of the microtubule-associated proteins. Proceedings of the National Academy of Sciences of the U.S.A. 78, 3413–3417.CrossRefGoogle ScholarPubMed
Jameson, L., Frey, T., Zeeberg, B., Dalldorf, F. & Caplow, M. (1980). Inhibition of microtubule assembly by phosphorylation of microtubule-associated proteins. Biochemistry 19, 2472–2479.CrossRefGoogle ScholarPubMed
Katz, L.C., Gilbert, C.D. & Wiesel, T.N. (1989). Local circuits and ocular dominance in monkey striate cortex. Journal of Neuroscience 9, 1389–1399.CrossRefGoogle ScholarPubMed
Kosofsky, B.E., Molliver, M.E., Morrison, J.H. & Foote, S.L. (1984). The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey (Macaca fascicularis). Journal of Comparative Neurology 230, 168–178.CrossRefGoogle ScholarPubMed
Kuljis, R.O. & Rakic, P. (1989). Neuropeptide Y-containing neurons are situated outside cytochrome-oxidase puffs in macaque visual cortex. Visual Neuroscience 2, 57–62.CrossRefGoogle ScholarPubMed
Laser, R.J. (1981). The dynamic ordering of neuronal cytoskeletons. Neuroscience Research Progress Bulletin 19, 7–31.Google Scholar
Leterrier, J.F., Liem, R.K.H. & Shelanski, M.L. (1982). Interactions between neurofilaments and microtubule-associated proteins: A possible mechanism for intraorganelle bridging. Journal of Cell Biology 95, 982–986.CrossRefGoogle Scholar
Levay, S., Hubel, D.H. & Wiesel, T.N. (1975). The pattern of ocular-dominance columns in macaque visual cortex revealed by a reduced silver stain. Journal of Comparative Neurology 159, 559–576.CrossRefGoogle ScholarPubMed
Lidow, M.S., Goldman-Rakic, P.S., Gallagher, D.W. & Rakic, P. (1991). Distribution of dopaminergic receptors in the primate cerebral cortex: Quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone, and [3H]SCH23390. Neuroscience 40, 657–671.CrossRefGoogle Scholar
Lidow, M.S., Gallagher, D.W., Rakic, P. & Goldman-Rakic, P.S. (1989). Regional differences in the distribution of muscarinic cholinergic receptors in the macaque cerebral cortex. Journal of Comparative Neurology 289, 247–259.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 U.S.A. 79, 6098–6101.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1983). Specificity of cortico-cortical connections in monkey visual system. Nature 304, 531–534.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatto). Journal of Comparative Neurology 147, 455–496.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Lund, J.S., Boothe, R.G. & Lund, R.D. (1977). Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): a Golgi study from fetal day 127 to postnatal maturity. Journal of Comparative Neurology 176, 149–188.CrossRefGoogle ScholarPubMed
Malach, R. (1990). Dendritic arborizations of visual cortex neurons and their relation to the cytochrome oxidase (CO) rich blobs in monkey striate cortex. Society for Neuroscience Abstracts 16, 292.Google Scholar
Malach, R. (1991). Relationship of biocytin labeled neuronal processes to the cytochrome oxidase (CO) rich blobs in monkey striate cortex. Society for Neuroscience Abstracts 17, 117.Google Scholar
Malach, R. (1992). Dendritic sampling across processing streams in monkey striate cortex. Journal of Comparative Neurology 315, 303–312.CrossRefGoogle ScholarPubMed
Mates, S.L. & Lund, J.S. (1983). Spine formation and maturation of type 1 synapses on spiny stellate neurons in primate visual cortex. Journal of Comparative Neurology 221, 91–97.CrossRefGoogle ScholarPubMed
Matus, A. (1987). Putting together the neuronal cytoskeleton. Trends in Neuroscience 10, 186–188.CrossRefGoogle Scholar
Matus, A. (1988). Microtubule-associated proteins: Their potential role in determining neuronal morphology. Annual Review of Neuroscience 11, 29–44.CrossRefGoogle ScholarPubMed
Matus, A., Bernhardt, R. & Hugh-Jones, T. (1981). High molecular weight microtubule-associated proteins are preferentially associated with dendritic microtubules in brain. Proceedings of the National Academy of Sciences of the U.S.A. 78, 3010–3014.CrossRefGoogle ScholarPubMed
Matus, A. & Riederer, B. (1986). Microtubule-associated proteins in the developing brain. Annals of the New York Academy of Science 466, 167–179.CrossRefGoogle ScholarPubMed
Morrison, J.H., Foote, S.L., Molliver, M.E., Bloom, F.E. & Lidov, H.G.W. (1982). Noradrenergic and serotonergic fibers innervate complementary layers in monkey primary visual cortex: An immunohistochemical study. Proceedings of the National Academy of Sciences of the U.S.A. 79, 2401–2405.CrossRefGoogle ScholarPubMed
Murphy, A.S.N. & Flavin, M. (1983). Microtubule assembly using the microtubule-associated protein MAP2 prepared in defined states of phosphorylation with protein kinase and phosphatase. European Journal of Biochemistry 137, 37–46.CrossRefGoogle Scholar
Murphy, D.B. & Borisy, G.G. (1975). Association of high-molecularweight proteins with microtubules and their role in microtubule assembly in vitro. Proceedings of the National Academy of Sciences of the U.S.A. 72, 2696–2700.CrossRefGoogle Scholar
Murphy, D.B., Johnson, J.A. & Borisy, G.G. (1977). Role of tubulin-associated proteins in microtubule nucleation and elongation. Journal of Molecular Biology 117, 33–52.CrossRefGoogle ScholarPubMed
Peters, A. & Sethares, C. (1991 a). Organization of pyramidal neurons in area 17 of monkey visual cortex. Journal of Comparative Neurology 306, 1–23.CrossRefGoogle ScholarPubMed
Peters, A. & Sethares, C. (1991 b). Layer IVA of Rhesus monkey primary visual cortex. Cerebral Cortex 1, 445–462.CrossRefGoogle ScholarPubMed
Rakic, P., Goldman-Rakic, P.S. & Gallagher, D. (1988). Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex. Journal of Neuroscience 8, 3670–3690.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Lund, J.S. (1983). Intrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 303–318.CrossRefGoogle ScholarPubMed
Rosier, A.M., Orban, G.A. & Vandesande, F. (1990). Regional distribution of binding sites for neuropeptide Y in cat and monkey visual cortex determined by in vitro receptor autoradiography. Journal of Comparative Neurology 293, 486–498.CrossRefGoogle Scholar
Ruiz-Marcos, A. & Valverde, F. (1969). The temporal evolution of the distribution of dendritic spines in the visual cortex of normal and dark-reared mice. Experimental Brain Research 8, 284–294.CrossRefGoogle Scholar
Sandell, J.H. (1986). NADPH diaphorase histochemistry in the macaque striate cortex. Journal of Comparative Neurology 251, 388–397.CrossRefGoogle ScholarPubMed
Shaw, C. & Cynader, M.C. (1986). Laminar distribution of receptors in monkey (Macaca fascicularis) geniculostriate system. Journal of Comparative Neurology 248, 301–312.CrossRefGoogle ScholarPubMed
Sloboda, R.D., Dentler, W.L. & Rosenbaum, J.L. (1976). Microtubule-associated proteins and stimulation of tubulin assembly in vitro. Biochemistry 15, 4497–4505.CrossRefGoogle ScholarPubMed
Tigges, M., Tioces, J., Mcdonald, J.K., Slattery, M. & Fernandes, A. (1989). Postnatal development of neuropeptide Y-like immunoreactivity in area 17 of normal and visually deprived rhesus monkeys. Visual Neuroscience 2, 315–328.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Hamilton, S.L., Silverman, M.S. & Switkes, E. (1988 a). Functional anatomy of macaque striate cortex. 1. Ocular dominance, binocular interactions and baseline conditions. Journal of Neuroscience 8, 1500–1530.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., De Valois, R.L. & Switkes, E. (1988 b). Functional anatomy of macaque striate cortex. 111. Color. Journal of Neuroscience 8, 1569–1593.CrossRefGoogle Scholar
Tootell, R.B.H., Hamilton, S.L. & Switkes, E. (1988C). Functional anatomy of macaque striate cortex. IV. Contrast and magno-parvo streams. Journal of Neuroscience 8, 1594–1609.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L. & De Valois, R.L. (1988d). Functional anatomy of macaque striate cortex. V. Spatial frequency. Journal of Neuroscience 8, 1610–1624.CrossRefGoogle ScholarPubMed
Trojanowski, J.Q., Schuck, T., Schmidt, L. & Lee, V.M.-Y. (1989). Distribution of phosphate-independent MAP 2 epitopes revealed with monoclonal antibodies in microwave-denatured human nervous system tissues. Journal of Neuroscience Methods 29, 171–180.CrossRefGoogle ScholarPubMed
Trusk, T.C., Kaboord, W.S. & Wono-Riley, M.T.T. (1990). Effects of monocular enucleation, tetrodotoxin, and lid suture on cytochrome-oxidase reactivity in supragranular puffs of adult macaque striate cortex. Visual Neuroscience 4, 185–204.CrossRefGoogle ScholarPubMed
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8, 1712–1727.CrossRefGoogle ScholarPubMed
Valverde, F. (1971). Rate and extent of recovery from dark rearing in the visual cortex of the mouse. Brain Research 33, 1–11.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. & Carroll, E.W. (1984). Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262CrossRefGoogle ScholarPubMed