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Functional architecture of area 17 in normal and monocularly deprived marmosets (Callithrix jacchus)

Published online by Cambridge University Press:  02 June 2009

Frank Sengpiel ,
David Troilo ,
Peter C. Kind ,
Bryan Graham  and
Colin Blakemore
Frank Sengpiel
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford OX1 3PT, UK
David Troilo
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford OX1 3PT, UK
Peter C. Kind
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford OX1 3PT, UK
Bryan Graham
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford OX1 3PT, UK
Colin Blakemore
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford OX1 3PT, UK
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Abstract

The organization of the primary visual cortex (VI) of the common marmoset (Callithrix jacchus) was studied both physiologically and by means of transneuronal labelling of geniculocortical afferents. We addressed the question whether monocular deprivation (MD) could stabilize segregation into ocular dominance (OD) columns, which are not seen in normal adult marmosets but are present in juvenile animals (Spatz, 1979, 1989). Properties of neurons in normal marmosets closely resembled those of other New-World and Old-World monkeys and orderly tangential progressions of preferred orientation were observed. However, in contrast to species that display well-defined OD columns, neurons of layer 4 in VI of normal adult marmosets received balanced inputs from the two eyes. Early MD (even though followed by prolonged binocular experience into adulthood) resulted in a reduction of cell size in laminae of the lateral geniculate nucleus with input from the deprived eye and a dramatic overall shift in ocular dominance towards the non-deprived eye in the cortex. However, isolated clusters of cells dominated by the deprived eye were found in both layers 4 and 6. Injection of lectin-conjugated horseradish peroxidase (WGA-HRP) into the deprived eye revealed elongated patches of terminal label, about 350 μm wide, in flat-mounted sections through layer 4. Afferent segregation was sharper and more regular in the region of VI representing parafoveal visual space than in that representing the fovea. Our findings support the notion that all Old-World and New-World monkeys possess the capacity for segregation of geniculocortical afferents into OD columns.

Keywords

New-World monkeyMarmosetPrimary visual cortexOcular dominance columnsMonocular deprivationOrientation columns
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 145 - 160
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Anderson, P.A., Olavarria, J. & Van Sluyters, R.C. (1988). The overall pattern of ocular dominance bands in cat visual cortex. Journal of Neuroscience 8, 2183–2200.CrossRefGoogle ScholarPubMed
Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth perception. Journal of Physiology 193, 327–342.CrossRefGoogle Scholar
Blakemore, C. (1988). The sensitive periods of the monkey's visual cortex. In Strabismus and Amblyopia, Vol. 49, Wenner-Gren International Symposium Series, ed. Lennerstrand, G., Von Noorden, G.K., Campos, E.C., pp. 219–234. London: Macmillan Press.CrossRefGoogle Scholar
Blakemore, C. & Van Sluyters, R.C. (1975). Innate and environmental factors in the development of the kitten's visual cortex. Journal of Physiology 248, 663–716.CrossRefGoogle ScholarPubMed
Blakemore, C., Garey, L.J. & Vital-Durand, F. (1978). The physiological effects of monocular deprivation and their reversal in the monkey's visual cortex. Journal of Physiology 283, 223–262.CrossRefGoogle ScholarPubMed
Blakemore, C., Vital-Durand, F. & Garey, L.J. (1981). Recovery from monocular deprivation in the monkey. 1. Reversal of physiological effects in the visual cortex. Proceedings of the Royal Society B (London) 213, 399–423.Google Scholar
Blasdel, G.G. & Salama, G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585.CrossRefGoogle ScholarPubMed
Bonhoeffer, T. & Grinvald, A. (1991). Iso-orientation domains in cat visual cortex are arranged in pinwheel-like pattern. Nature 353, 429–431.CrossRefGoogle Scholar
Brodmann, K. (1909). Vergleichende Lokalisatlonslehre der GroÞihirn-rinde. Leipzig: Barth.Google Scholar
Casagrande, V.A. & Harting, J.K. (1975). Transneuronal transport of tritiated fucose and proline in the visual pathways of the tree shrew, Tupaia glis. Brain Research 96, 367–372.CrossRefGoogle ScholarPubMed
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, 315.Google Scholar
Constantine-Paton, M. & Law, M.I. (1978). Eye-specific termination bands in tecta of three-eyed frogs. Science 202, 639–641.CrossRefGoogle ScholarPubMed
DeBruyn, E.J. & Casagrande, V.A. (1981). Demonstration of ocular dominance columns in a New World primate by means of monocular deprivation. Brain Research 207, 453–458.CrossRefGoogle Scholar
Dörsteler, M.R., Garey, L.J. & Movshon, J.A. (1976). Reversal of the morphological effects of monocular deprivation in the kitten's lateral geniculate nucleus. Journal of Physiology 261, 189–210.CrossRefGoogle Scholar
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
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
Friedlander, M.J., Martin, K.A.C. & Wassenhove-McCarthy, D. (1991). Effects of monocular visual deprivation on geniculocorti-cal innervation of area 18 in cat. Journal of Neuroscience 11, 3268–3288.CrossRefGoogle ScholarPubMed
Fritschy, J.M. & Garey, L.J. (1986). Quantitative changes in morphological parameters in the developing visual cortex of the marmoset monkey. Developmental Brain Research 29, 173–188.CrossRefGoogle Scholar
Glendenning, K.K., Kofron, E.A. & Diamond, I.T. (1976). Laminar organization of projections of the lateral geniculate nucleus to the striate cortex in Galago. Brain Research 105, 538–546.CrossRefGoogle Scholar
Glickstein, M. & Millodot, M. (1970). Retinoscopy and eye size. Science 168, 605–606.CrossRefGoogle ScholarPubMed
Hassler, R. & Wagner, A. (1965). Experimentelle und morphologische Befunde über die vierfache corticale Projektion des visuellen Systems. Proceedings of the 8th International Congress of Neurology 3, 77–96.Google Scholar
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
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in New and Old World primates. Journal of Comparative Neurology 182, 123–136.CrossRefGoogle Scholar
Hendrickson, A.E. & Wilson, J.R. (1979). A difference in 14C-deoxyglucose autoradiographic patterns in striate cortex between Macaca and Saimiri monkeys following monocular stimulation. Brain Research 170, 353–358.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
Hitchcock, P.F. & Hickey, T.L. (1980). Ocular dominance columns: Evidence for their presence in humans. Brain Research 182, 176–179.CrossRefGoogle ScholarPubMed
Horton, J.C. & Hedley-Whyte, E.T. (1984). Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philosophical Transactions of the Royal Society (London) 304, 255–272.Google ScholarPubMed
Hubel, D.H. (1975). An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis). Brain Research 96, 41–50.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 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
Hubel, D.H. & Wiesel, T.N. (1974). Sequence regularity and geometry of orientation columns in the monkey striate cortex. Journal of Comparative Neurology 158, 267–293.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
Hubel, D.H. & Wiesel, T.N. (1978). Distribution of inputs from the two eyes to striate cortex of squirrel monkeys. Society for Neuroscience Abstracts 4, 632.Google Scholar
Hubel, D.H., Wiesel, T.N. & LeVay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society (London) 278, 377–409.Google ScholarPubMed
Illing, R.-B. & Wässle, H.(1979). Visualization of the HRP reaction product using the polarization microscope. Neuroscience Letters 13, 7–11.CrossRefGoogle ScholarPubMed
LeVay, S., Connolly, M., Houde, J. & Van Essen, D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience 5, 486–501.CrossRefGoogle ScholarPubMed
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
LeVay, S., Stryker, M.P. & Shatz, C.J. (1978). Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study. Journal of Comparative Neurology 179, 223–244.CrossRefGoogle ScholarPubMed
LeVay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191, 1–51.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
Löwel, S. & Singer, W. (1993). Monocularly induced 2–deoxyglucose patterns in the visual cortex and lateral geniculate nucleus of the cat: II. Awake animals and strabismic animals. European Journal of Neuroscience 5, 857–869.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.CrossRefGoogle ScholarPubMed
Mower, G.D. & Christen, W.G. (1989). Evidence for an enhanced role of G ABA inhibition in visual cortical ocular dominance of cats reared with abnormal monocular experience. Developmental Brain Research 45, 211–218.CrossRefGoogle Scholar
Obermayer, K. & Blasdel, G.G. (1993). Geometry of orientation and ocular dominance columns in monkey striate cortex. Journal of Neuroscience 13, 4114–4129.CrossRefGoogle ScholarPubMed
Price, D.J., Ferrer, J.M.R., Blakemore, C. & Kato, N. (1994). Functional organization of corticocortical projections from area 17 to area 18 in the cat's visual cortex. Journal of Neuroscience 14, 2732–2746.CrossRefGoogle ScholarPubMed
Rakic, P. (1976). Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261, 467–471.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Gattas, R. & Fiorani, M. Jr. (1988). Complete pattern of ocular dominance stripes in VI of a New World monkey, Cebus apella. Experimental Brain Research 72, 645–648.CrossRefGoogle Scholar
Rosa, M.G.P., Gattas, R. & Fiorani, M. Jr. (1992). Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex of Cebus monkeys. Experimental Brain Research 88, 249–264.CrossRefGoogle ScholarPubMed
Rowe, M.H., Benevento, L.A. & Rezak, M. (1978). Some observations on the pattern of segregated geniculate inputs to the visual cortex in New World primates: An autoradiographic study. Brain Research 159, 371–378.CrossRefGoogle Scholar
Schiller, P.H., Finlay, B.L. & Volman, S.F. (1976). Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. Journal of Neurophysiology 39, 1320–1333.CrossRefGoogle ScholarPubMed
Senopiel, F., Troilo, D. & Blakemore, C. (1992). Functional architecture of primary visual cortex in normal and monocularly deprived common marmosets. Investigative Ophthalmology and Visual Science 33, 1217.Google Scholar
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. Journal of Physiology 281, 267–283.CrossRefGoogle ScholarPubMed
Shatz, C.J., Lindström, S. & Wiesel, T.N. (1977). The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Research 131, 103–116.CrossRefGoogle ScholarPubMed
Sillito, A.M., Kemp, J.A. & Blakemore, C. (1981). The role of GABA-ergic inhibition in the cortical effects of monocular deprivation. Nature 291, 318–320.CrossRefGoogle Scholar
Spatz, W.B. (1978). The retino-geniculo-cortical pathway in Callithrix. I. Intraspecific variations in the lamination pattern of the lateral geniculate nucleus. Experimental Brain Research 33, 551–563.CrossRefGoogle ScholarPubMed
Spatz, W.B. (1979). The retino-geniculo-cortical pathway in Callithrix. II. The geniculo-cortical projection. Experimental Brain Research 36, 401–410.CrossRefGoogle ScholarPubMed
Spatz, W.B. (1989). Loss of ocular dominance columns with maturity in the monkey, Callithrix jacchus. Brain Research 488, 376–380.CrossRefGoogle ScholarPubMed
Stephan, H., Baron, G. & Schwerdtfeger, W.K. (1980). The Brain of the Common Marmoset: A Stereotaxic Atlas. Berlin: Springer.Google Scholar
Swindale, N.V. (1980). A model for the formation of ocular dominance stripes. Proceedings of the Royal Society B (London) 208, 243–264.Google Scholar
Swindale, N.V., Vital-Durand, F. & Blakemore, C. (1981). Recovery from monocular deprivation in the monkey. III. Reversal of anatomical effects in the visual cortex. Proceedings of the Royal Society B (London) 213, 435–450.Google ScholarPubMed
Tigges, J. & Tigges, M. (1979). Ocular dominance columns 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
Tigges, J., Tigges, M. & Perachio, A.A. (1977). Complementary laminar termination of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey. Journal of Comparative Neurology 176, 87–100.CrossRefGoogle ScholarPubMed
Troilo, D. & Judge, S.J. (1993). Ocular development and visual deprivation myopia in the common marmoset (Callithrix jacchus). Vision Research 33, 1311–1324.CrossRefGoogle ScholarPubMed
von der Malsburg, C. (1979). Development of ocularity domains and growth behaviour of axon terminals. Biological Cybernetics 32, 49–62.CrossRefGoogle ScholarPubMed
Würgötter, F. & Eysel, U.T. (1987). Quantitative determination of orientational and directional components in the response of visual cortical cells to moving stimuli. Biological Cybernetics 57, 349–355.CrossRefGoogle Scholar