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The distribution of corticotectal projection neurons correlates with the interblob compartment in macaque striate cortex

Published online by Cambridge University Press:  02 June 2009

Barry Lia  and
Jaime F. Olavarria
Barry Lia
Affiliation:
Department of Psychology, University of Washington, Seattle
Jaime F. Olavarria
Affiliation:
Department of Psychology, University of Washington, Seattle
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Abstract

While much attention has been given to the correlation between cytochrome-oxidase (CO) compartments and patterns of cortico-cortical projections originating from supragranular layers in the striate cortex, little is known in this regard about patterns of cortico-subcortical projections originating from infragranular cortex. We studied the tangential distribution of the striate cortex neurons projecting to the superior colliculus and used two approaches to analyze the relationship of this distribution to the arrangement of CO “blobs.” First, chi-square analysis indicated that significantly fewer labeled neurons were found within the CO blob compartment than the number expected for a random distribution. Second, spatial cross-correlation analysis – which circumvents the inherent subjectivity of delineating blob boundaries – revealed an area around blob centers in which there was a decreased probability of encountering labeled cells. The size of this area compared well with that of our outlines of CO blobs. We conclude that corticotectal projection neurons in the striate cortex are distributed preferentially within the interblob compartment of the infragranular striate cortex. These results demonstrate that the spatial distribution of cortico-subcortical projection neurons within infragranular cortex can correlate with the CO architecture of the primary visual cortex.

Keywords

Superior colliculusCytochrome-oxidase architectureParallel pathwaysSubcorticalInfragranular
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 3 , May 1996 , pp. 461 - 466
Copyright
Copyright © Cambridge University Press 1996

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References

Abel, P.L., O'BRIEN, B.J., Lia, B. & Olavarria, J.F. (1994). The distribution of cortico-collicular projection neurons correlates with thick cytochrome oxidase stripes in visual area V2 of macaque monkey. Society for Neuroscience Abstracts 20, 1741.Google Scholar
Blasdel, G.G., Lund, J.S. & Fitzpatrick, D. (1985). Intrinsic connections of macaque striate cortex: Axonal projections of cells outside lamina 4C. Journal of Neuroscience 5, 3350–3369.CrossRefGoogle ScholarPubMed
Casagrande, V.A. (1994). A third parallel visual pathway to primate area VI. Trends in Neurosciences 17, 305–309.CrossRefGoogle Scholar
Casanova, C. (1993). Response properties of neurons in area 17 projecting to the striate-recipient zone of the cat's lateralis posterior-pulvinar complex: Comparison with cortico-tectal cells. Experimental Brain Research 96, 247–259.CrossRefGoogle Scholar
Curcio, C.A. & Harting, J.K. (1978). Organization of pulvinar afferents to area 18 in the squirrel monkey: Evidence for stripes. Brain Research 143, 155–161.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neurosciences 11, 219–226.CrossRefGoogle ScholarPubMed
Deyoe, E.A., Felleman, D.J., Van Essen, D.C. & Mcclendon, E. (1994). Multiple processing streams in occipitotemporal visual cortex. Nature 371, 151–154.CrossRefGoogle ScholarPubMed
Ferrera, V.P., Nealey, T.A. & Maunsell, J. H.R. (1994). Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways. Journal of Neuroscience 14, 2080–2088.CrossRefGoogle ScholarPubMed
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., Usrey, W.M., Schofield, B.R. & Einstein, G. (1994). The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex. Visual Neuroscience 11, 307–315.CrossRefGoogle ScholarPubMed
Fries, W. & Distel, H. (1983). Large layer VI neurons of monkey striate cortex (Meynert cells) project to the superior colliculus. Proceedings of the Royal Society B (London) 219, 53–59.Google Scholar
Fries, W. (1984). Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase. Journal of Comparative Neurology 230, 55–76.CrossRefGoogle Scholar
Fries, W., Keizer, K. & Kuypers, H. G.J.M. (1985). Large layer VI cells in macaque striate cortex (Meynert cells) project to both superior colliculus and prestriate visual area V5. Experimental Brain Research 58, 613–616.CrossRefGoogle ScholarPubMed
Fries, W. (1986). Distribution of Meynert cells in primate striate cortex. Naturwissenschaften 73, 557–558CrossRefGoogle ScholarPubMed
Hendrickson, A.E. (1985). Dots, stripes and columns in monkey visual cortex. Trends in Neurosciences 8, 406–410.CrossRefGoogle Scholar
Hendry, S. H.C. (1994). A neurochemically distinct third channel in the macaque lateral geniculate nucleus. In Thalamic Networks for Relay and Modulation, ed. Minciacchi, D., Molinari, M., Macchi, G. & Jones, E.G., pp. 251–265. Oxford, England: Pergamon Press.Google Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199–253.Google ScholarPubMed
Lachica, E.A., Beck, P.O. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the U.S.A. 89, 3566–3570.CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.O. & Casagrande, V.A. (1993). Intrinsic connections of layer III of striate cortex in squirrel monkey and bush baby: Correlations with patterns of cytochrome oxidase. Journal of Comparative Neurology 329, 163–187.CrossRefGoogle ScholarPubMed
Levitt, J.B., Yoshioka, T. & Lund, J.S. (1995). Connections between the pulvinar complex and cytochrome oxidase-defined compartments in visual area V2 of macaque monkey. Experimental Brain Research 104, 419–430.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. (1984 a). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 b). Specificity of intrinsic connections in primate visual cortex. Journal of Neuroscience 4, 2830–2835.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1987). Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey. Journal of Neuroscience 7, 3371–3377.CrossRefGoogle ScholarPubMed
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
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, 287–303.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 253–288.CrossRefGoogle ScholarPubMed
Martin, K. A.C. (1988). From enzymes to visual perception: A bridge too far? Trends in Neurosciences 11, 380–387.CrossRefGoogle ScholarPubMed
Maunsell, J. H.R. (1987). Physiological evidence for two visual subsystems. In Matters of Intelligence, ed. Vaina, L. M., pp. 59–87. Dortrecht, Netherlands: D. Reidel Publishing Company.CrossRefGoogle Scholar
Merigan, W.H. & Maunsell, J. H.R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369–402.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1978). Tetramethylbenzidine 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 Scholar
Nealey, T.A. & Maunsell, J. H.R. (1994). Magnocellular and parvo-cellular contributions to the responses of neurons in macaque striate cortex. Journal of Neuroscience 14, 2069–2079.CrossRefGoogle Scholar
Olavarria, J. & Van Sluyters, R.C. (1985). Unfolding and flattening the cortex of gyrencephalic brains. Journal of Neuroscience Methods 15, 191–202.CrossRefGoogle ScholarPubMed
Olavarria, J.F. & Lia, B. (1993). The distribution of cortico-collicular projection neurons correlates with cytochrome oxidase architecture in striate cortex of macaque monkey. Society for Neuroscience Abstracts 19, 334.Google Scholar
Payne, B.R. & Peters, A. (1989). Cytochrome oxidase patches and Meynert cells in monkey visual cortex. Neuroscience 28, 353–363.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1991). The density recovery profile: a method for the analysis of points in the plane applicable to retinal studies. Visual Neuroscience 6, 95–111.CrossRefGoogle ScholarPubMed
Schiller, P.H., Malpeli, J.G. & Schein, S.J. (1979). Composition of geniculostriate input to superior colliculus of the rhesus monkey. Journal of Neurophysiology 42, 1124–1133.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Logothetis, N.K. (1990). The color-opponent and broad-band channels of the primate visual system. Trends in Neurosciences 13, 392–398.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S. (1989). The organization of connections between areas V5 and VI in macaque monkey visual cortex. European Journal of Neuroscience 1, 309–332.CrossRefGoogle Scholar
Tootell, R. B.H., Silverman, M.S., Hamilton, S.L., De Valois, R.L. & Switkes, E. (1988). Functional anatomy of macaque striale cortex. III. Color. Journal of Neuroscience 8, 1569–1593.CrossRefGoogle Scholar
Trojanowski, J.Q. & Jacobson, S. (1977). The morphology and laminar distribution of cortico-pulvinar neurons in the rhesus monkey. Experimental Brain Research 28, 51–62.Google ScholarPubMed
Usrey, W.M. & Fitzpatrick, D. (1994). Laminar specificity in the relay of magnocellular and parvocellular streams to the superficial and deep layers of macaque striate cortex. Society for Neuroscience Abstracts 20, 1578.Google Scholar
Van Essen, D.C., Felleman, D.J., Deyoe, E.A., Olavarria, J. & Knierim, J. (1990). Modular and hierarchical organization of extra-striate visual cortex in the macaque monkey. Cold Springs Harbor Symposia on Quantitative Biology LV, 679–696.CrossRefGoogle Scholar
Weller, R.E. (1988). Two cortical visual systems in Old World and New World primates. Progress in Brain Research 75, 293–306.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. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neurosciences 12, 94–101.CrossRefGoogle ScholarPubMed
Yoshioka, T., Levitt, J.B. & Lund, J.S. (1994). Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections. Visual Neuroscience 11, 467–489.CrossRefGoogle ScholarPubMed
Zeki, S. & Shipp, S. (1988). The functional logic of cortical connections. Nature 335, 311–317.CrossRefGoogle ScholarPubMed