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Neurochemical compartmentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species

Published online by Cambridge University Press:  02 June 2009

Stewart H. C. Hendry  and
Renee K. Carder
Stewart H. C. Hendry
Affiliation:
Zanvyl Krieger Mind/Brain Institute and Department of Neuroscience, Johns Hopkins University, Baltimore
Renee K. Carder
Affiliation:
Department of Psychology, University of California at Los Angeles, Los Angeles
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Abstract

The compartmental organization of visual cortical neurons was examined across species of primates by directly comparing the pattern of immunoreactivity for the 28-kD vitamin D-dependent calcium-binding protein (calbindin) in area 17 of squirrel monkeys, macaques, and neurologically normal adult humans. Area 17 of macaques and squirrel monkeys was similar in that somata and processes intensely immunoreactive for calbindin were present in the same layers (II-III, IVB, and V) and in both species formed a well-stained matrix that surrounded the CO-rich puffs in layer III. These intensely calbindin-immunoreactive neurons were identified as subpopulations of GABA-immunoreactive neurons. Among the most obvious differences in the two monkey species was the distribution of calbindin-positive elements outside of layer III: a dense immunostained matrix surrounded the puffs in layers II, IVB, V, and VI of squirrel monkeys but the immunostained neurons adopted no regular pattern outside layer III in macaques. In addition, although somata lightly immunoreactive for calbindin were present in both species, they were much more abundant in squirrel monkeys than macaques. The pattern of calbindin immunostaining in human area 17 resembled that of macaques in forming an intense matrix that surrounded puffs only in layer III, yet also resembled that of squirrel monkeys by including large numbers of lightly immunoreactive somata. These lightly immunostained somata included a very dense population forming a prominent band in layer IVA of human visual cortex. We conclude that for layer III of primary visual cortex, a similar pattern of neuronal chemistry exists across species of primates which is related to this layer's compartmental organization. Yet for other layers, the expression of calbindin immunoreactivity varies from one species to the next, perhaps reflecting variations in other neuronal properties.

Keywords

Calcium-binding proteinStriate cortexCytochrome-oxidase puffsGABA neurons
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 6 , November 1993 , pp. 1109 - 1120
Copyright
Copyright © Cambridge University Press 1993

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References

Allman, J. & Zucker, S. (1990). Cytochrome o.xidase and functional coding in primate striate cortex: A hypothesis. Cold Spring Harbor Symposium on Quantitative Biology 55, 979–982.CrossRefGoogle ScholarPubMed
Beaulieu, C, Kisvarday, Z., Somogyi, P., Cynader, M. & Cowey, A. (1992). Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cerebral Cortex 2, 295–309.CrossRefGoogle ScholarPubMed
Billings-Gagliardi, S., Chan-Palay, V. & Palay, S.L. (1974). A review of lamination in area 17 of the visual cortex in Macaca mulatto. Journal of Neurocytology 3, 619–629.CrossRefGoogle Scholar
Blümcke, I., Hof, P.R., Morrison, J.H. & Celio, M.R. (1990). Distribution of parvalbumin immunoreactivity in the visual cortex of Old World monkeys and humans. Journal of Comparative Neurology 301, 417–432.CrossRefGoogle ScholarPubMed
Brodmann, K. (1909). Vergleichende Lokalisationehre der Groβhirnrinde in ihrn Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: J. A. Barth.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 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
Carroll, E.W. & Wong-Riley, M.T.T. (1984). Quantitative light- and electron-microscopic analyses of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkeys. Journal of Comparative Neurology 222, 1–17.CrossRefGoogle Scholar
Casagrande, V.A. & DeBruyn, E.J. (1982). The galago visual system: Aspects of normal organization and developmental plasticity. In The Lesser Bushbaby (Galago) as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 137–168. Boca Raton, Florida: CRC Press.Google Scholar
Casagrande, V.A. & Skeen, L.C. (1980). Organization of ocular-dominance columns in galago demonstrated by autoradiographic and deoxyglucose methods. Society for Neuroscience Abstracts 6, 113.Google Scholar
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
Christakos, S., Gabrielides, C. & Rhoten, W.B. (1989). Vitamin D-dependent calcium-binding proteins: Chemistry, distribution, functional considerations, and molecular biology. Endocrinology Review 10, 3–26.CrossRefGoogle ScholarPubMed
Clarke, S. & Miklossy, J. (1990). Occipital cortex in man: Organization of callosal connections, related myelo- and cytoarchitectonics, and putative boundaries of functional visual areas. Journal of Comparative Neurology 298, 188–214.CrossRefGoogle Scholar
Cresho, H.S., Rasco, L.M., Rose, G.H. & Condo, G.J. (1992). Blob-like pattern of cytochrome oxidase staining in ferret visual cortex. Society for Neuroscience Abstracts 18, 298.Google Scholar
DeFelipe, J., Hendry, S., Hashikawa, T., Molinari, M. & Jones, E. (1991). A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37, 655–673.CrossRefGoogle Scholar
DeFelipe, J., Hendry, S.H.C. & Jones, E.G. (1989). Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Research 503, 49–54.CrossRefGoogle ScholarPubMed
DeFelipe, J. & Jones, E.G. (1992). High-resolution light- and electron-microscopic immunocytochemistry of co-localized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex. European Journal of Neuroscience 4, 46–60.CrossRefGoogle Scholar
De Lima, A.D. & Morrison, J.H. (1989). Ultrastructural analysis of somatostatin-immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey. Journal of Comparative Neurology 283, 212–227.CrossRefGoogle ScholarPubMed
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
Fisken, R.A., Garey, L.J. & Powell, T.P.S. (1975). The intrinsic, association, and commissural connections of area 17 of the visual cortex. Philosophical Transactions of the Royal Society B (London) 272, 487–536.Google 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., Schmechel, D. & Towles, A.W. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Florence, S.L., Conley, M. & Casagrande, V.A. (1986). Ocular-dominance columns and retinal projections in New World spider monkeys (Ateles ater). Journal of Comparative Neurology 243, 234–248.CrossRefGoogle ScholarPubMed
Florence, S.L. & Kaas, J.H. (1992). Ocular-dominance columns in area 17 of Old World macaque and talapoin monkeys: Complete reconstructions and quantitative analyses. Visual Neuroscience 8, 449–462.CrossRefGoogle ScholarPubMed
Hayes, T.L. & Lewis, D.A. (1992). Nonphosphorylated neurofilament protein and calbindin immunoreactivity in layer III pyramidal neurons of human neocortex. Cerebral Cortex 2, 56–67.CrossRefGoogle ScholarPubMed
Heizmann, C.W., Röhrenbeck, J. & Kamphuis, W. (1989). Parvalbumin, molecular, and functional aspects. In Calcium Binding Proteins in Normal and Transformed Cells, ed. Pochet, R., Lawson, D.E.M. & Heizmann, C.W., pp. 57–66. New York: Plenum Press.Google Scholar
Hendrickson, A.E. (1982). The orthograde axoplasmic transport autoradiographic technique and its implications for additional neuro-anatomical analysis of the striate cortex. In Cytochemical Methods in Neuroanatomy, ed. Chan-Palay, V. & Palay, S., 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
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., Van Brederode, J.F.M., Mulligan, K.A. & Celio, M.R. (1991). Development of the calcium-binding proteins parvalbumin and calbindin in monkey striate cortex. Journal of Comparative Neurology 307, 626–646.CrossRefGoogle ScholarPubMed
Hendry, S. & Carder, R.K. (1992). Organization and plasticity of GABA neurons and receptors in monkey visual cortex. In Progress in Brain Research, Volume 90, GABA in the Retina and Central Visual System, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 477–502. North Holland: Elsevier.Google Scholar
Hendry, S.H.C, Hockfield, S., Jones, E.G. & McKay, R. (1984 a). Monoclonal antibody that identifies subsets of neurons in the central visual system of monkey and cat. Nature 307, 267–269.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, Jones, E.G., Emson, P.C, Lawson, D.E.M., Heizmann, C.W. & Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium-binding protein immuno-reactivities. Experimental Brain Research 76, 467–472.CrossRefGoogle Scholar
Hess, D.T. & Edwards, M.A. (1987). Anatomical demonstration of ocular segregation in the retinogeniculocortical pathway of the New World capuchin monkey (Cebus apella). Journal of Comparative Neurology 264, 409–420.CrossRefGoogle ScholarPubMed
Hitchock, P.F. & Hickey, T.L. (1980). Ocular-dominance columns: Evidence for their presence in humans. Brain Research 182, 176–179.CrossRefGoogle Scholar
Hockfield, S., McKay, R.D., Hendry, S.H.C. & Jones, E.G. (1984). 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 35, 877–889.Google Scholar
Hockfield, S., Tootell, R.B.H. & Zaremba, S. (1990). Molecular differences among neurons reveal an organization of human visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 87, 3027–3031.CrossRefGoogle ScholarPubMed
Horton, J.C (1984). Cytochrome-oxidase patches: A new cytoarchi-tectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199–253.Google ScholarPubMed
Horton, J.C. (1990). Arrangement of ocular-dominance columns in human visual cortex. Archives of Ophthalmology 108, 1025–1031.CrossRefGoogle ScholarPubMed
Horton, J.C. & Hedley-Whtte, E.T. (1984). Mapping of cytochrome-oxidase patches and ocular-dominance columns in human visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 255–272.Google 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 geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
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
Kaas, J.H., Lin, C.S. & Casagrande, V.A. (1976). The relay of ipsi-lateral and contralateral retinal input from the lateral geniculate nucleus of primates. Journal of Comparative Neurology 106, 371–378.Google Scholar
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
Kretsinger, R.H. (1976). Calcium-binding proteins. Annual Review of Biochemistry 45, 239–266.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
Lachica, E.A. & Casagrande, V.A. (1992). Direct W-like geniculate projections to the cytochrome-oxidase (CO) blobs in primate visual cortex: Axon morphology. Journal of Comparative Neurology 319, 1–18.Google Scholar
Lledo, P., Somasundaram, B., Morton, A.J., Emson, P.C. & Mason, W.T. (1992). Stable transformation of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeosta-sis. Neuron 9, 943–954.CrossRefGoogle Scholar
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. & Yoshioka, T. (1991). Local circuit neurons of macaque monkey striate cortex: III. Neurons of laminae 4B, 4A, and 3B. Journal of Comparative Neurology 311, 234–258.CrossRefGoogle ScholarPubMed
Lund, J.S., Hawken, M.J. & Parker, A.J. (1988). Local circuit neurons of macaque monkey striate cortex: II. Neurons of laminae 5B and 6. Journal of Comparative Neurology 276, 1–29.CrossRefGoogle ScholarPubMed
Mattson, M.P., Rychlik, B., Chu, C. & Christakos, S. (1991). Evidence For calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron 6, 41–51.CrossRefGoogle ScholarPubMed
McGuinness, E., MacDonald, C, Sereno, M. & Allman, J. (1986). Primates without blobs: The distribution of cytochrome-oxidase activity in striate cortex of Tarsius, Haplemur, and Cheiragaleus. Society for Neuroscience Abstracts 12, 130.Google Scholar
Morrison, J.H. & Foote, S.L. (1986). Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. Journal of Comparative Neurology 243, 117–138.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, K.M., Van Sluyters, R.C. & Jones, D.G. (1990). Cytochrome-oxidase activity in cat visual cortex: Is it periodic? Society for Neuroscience Abstracts 16, 292.Google Scholar
Naegle, J.R. & Barnstable, C.J. (1989). Molecular determinants of GABAergic local-circuit neurons in the visual cortex. Trends in Neuroscience 12, 28–34.CrossRefGoogle Scholar
Rockland, K.S. & Lund, J.S. (1983). Intrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 303–318.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Gattass, R. & Soares, J.G.M. (1991). A quantitative analysis of cytochrome oxidase-rich patches in the primary visual cortex of Cebus monkeys: Topographic distribution and effects of late monocular enucleation. Experimental Brain Research 84, 195–209.CrossRefGoogle ScholarPubMed
Somogyi, P. & Cowey, A. (1984). Double bouquet cells. In Cerebral Cortex, Volume 1: Cellular Components of the Cerebral Cortex, ed. Peters, A. & Jones, E.G., pp. 337–360. New York: Plenum Press.Google Scholar
Spatz, W.B. (1989). Loss of ocular-dominance columns with maturity in the monkey, Callithrix jacchus. Brain Research 488, 376–380.CrossRefGoogle ScholarPubMed
Tigges, J. & Tigges, M. (1979). Ocular dominance in the striate cortex of chimpanzee (Pan troglodytes). Brain Research 166, 386–390.CrossRefGoogle ScholarPubMed
Tigges, M., Hendrickson, A.E. & Tigges, J. (1984). Anatomical consequences of long-term monocular eyelid closure on lateral geniculate nucleus and striate cortex in squirrel monkey. Journal of Comparative Neurology 227, 1–13.CrossRefGoogle ScholarPubMed
Valverde, F. (1971). Short axon neuronal subsystems in the visual cortex of the monkey. International Journal of Neuroscience 1, 181–197.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Van Eldk, L.Y., Zendegui, J.G., Marshak, D.R. & Watterson, D.M. (1982). Calcium-binding proteins and the molecular basis of calcium action. International Review of Cytology 77, 1–61.CrossRefGoogle Scholar
Von Bonin, G. (1942). The striate area of primates. Journal of Comparative Neurology 77, 405–429.CrossRefGoogle Scholar
Weber, J.T., Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: Studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135–145.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & Carroll, E.W. (1984). Effect of impulse blockage on cytochrome-oxidase activity in monkey visual system. Nature 307, 262–264.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T., Hevner, R.F., Cutlan, R., Earnest, M., Egan, R., Frost, J. & Nguyen, T. (1993). Cytochrome oxidase in the human visual cortex: Distribution in the developing and adult brain. Visual Neuroscience 10, 41–58.CrossRefGoogle ScholarPubMed