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Architectonic subdivisions of the inferior pulvinar in New World and Old World monkeys

Published online by Cambridge University Press:  02 June 2009

Iwona Stepniewska  and
Jon H. Kaas
Iwona Stepniewska
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Jon H. Kaas
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
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Abstract

Architectonic subdivisions of the inferior pulvinar (PI) complex were delineated in New World owl and squirrel monkeys and Old World macaque monkeys. Brain sections were processed for Nissl substance, myelin, cytochrome oxidase (CO), acetylcholinesterase (AChE), calbindin-D28K (Cb), or with the monoclonal antibody Cat-301. In all three primates, we identified the posterior nucleus (PIp) and the medial nucleus (PIm) of previous reports, and divided the previously recognized central nucleus (PIc) into two subdivisions, medial (PIcm) and lateral (PIcl). Each nucleus had several features that allowed it to be readily distinguished. (1) PIp was dark in Cb, and moderately dark in AChE and CO preparations. (2) PIm was Cb light, and AChE and CO dark. (3) PIcm was Cb dark, and AChE and CO light. (4) PIcl was Cb moderate with a scattering of dark neurons, and moderately dark for AChE and CO. (5) In sections processed for Cat-301, PIm in macaque monkeys and PIcm and PIp in squirrel monkeys stained darkly, while little staining was apparent in owl monkeys. The results allowed subdivisions of the inferior pulvinar to be more clearly defined, homologized, and compared across taxa. All monkeys appear to have the same four subdivisions of the PI, although properties vary.

Keywords

Visual systemThalamusCat-301Calbindin

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1043 - 1060
Copyright
Copyright © Cambridge University Press 1997

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References

Allman, J.M., Kaas, J.H., Lane, R.H. & Miezin, F.M. (1972). A representation of the visual field in the inferior nucleus of the pulvinar in the owl monkey (Aotus trivirgatus). Brain Research 40, 291–302.CrossRefGoogle ScholarPubMed
Beck, P.D. & Kaas, J.H. (1996). Subcortical connections with the dorsomedial visual cortical area (DM) in prosimian, New World and Old World primates. Society for Neuroscience Abstracts, 22, 1817.Google Scholar
Bender, D.B. (1981). Retinotopic organization of macaque pulvinar. Journal of Neurophysiology 46, 672–693.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Fallon, J.H. (1975). The ascending projections of the superior colliculus in the rhesus monkey (Macaco mulatto). Journal of Comparative Neurology 160, 339–362.CrossRefGoogle Scholar
Benevento, L.A. & Standage, G.P. (1983). The organization of projections of the retinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307–336.CrossRefGoogle Scholar
Boussaoud, D., Desimone, R. & Ungerleider, L.G. (1992). Subcortical connections of visual areas MST and FST in macaques. Visual Neuroscience 9, 291–302.CrossRefGoogle ScholarPubMed
Bullier, J., Girard, P. & Salin, P.A. (1994). The role of area 17 in the transfer of information to extrastriate visual cortex. In Cerebral Cortex ed. Peters, A. & Rockland, K.S., pp. 301–331. New York: Plenum.Google Scholar
Campos-Ortega, J.A. & Hayhow, W.R. (1972). On the organization of the visual cortical projection to the pulvinar in Macaco mulatto. Brain, Behaviour, and Evolution 6, 394–423.CrossRefGoogle Scholar
Casagrande, V.A. & Kaas, J.H. (1994). The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In Cerebral Cortex, ed. Peters, A. & Rockland, K.S., pp. 201–259. New York: Plenum.Google Scholar
Celio, M.R. (1990). Calbindin D28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.CrossRefGoogle ScholarPubMed
Cowey, A. & Stoerig, P. (1995). Blindsight in monkeys. Nature 373, 247–249.CrossRefGoogle ScholarPubMed
Cusick, C.G., Scripter, J.L., Darensbourg, J.G. & Weber, J.T. (1993). Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr. Journal of Comparative Neurology 336, 1–30.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., 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
De Yoe, E.A., Trusk, T.C. & Wong-Riley, M.T.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 Scholar
Dick, A., Kaske, A. & Creutzfeld, O.D. (1991). Topographical and topological organization of the thalamocortical projection to the striate and prestriale cortex in the marmoset (Callithrix jacchus). Experimental Brain Research 84, 233–253.CrossRefGoogle Scholar
GallYas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203–209.CrossRefGoogle ScholarPubMed
Gattas, R., Oswaldo-Cruz, E. & Sousa, A.P.B. (1978). Visuotopic organization of the Cebus pulvinar: A double representation of the contralateral hemifield. Brain Research 152, 1–16.CrossRefGoogle Scholar
Geneser-Jensen, F.A. & Blackstad, T.W. (1971). Distribution of acetylcholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, parasubiculum, and presubiculum. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 114, 460–481.CrossRefGoogle ScholarPubMed
Graham, J. (1982). Some topographical connections of the striate cortex with subcortical structures in Macaca fascicularis. Experimental Brain Research 47, 1–14.CrossRefGoogle ScholarPubMed
Graham, J., Lin, C.-S. & Kaas, J.H. (1979). Subcortical projections of six visual cortical areas in owl monkey, Aotus trivirgatus. Journal of Comparative Neurology 187, 557–580.CrossRefGoogle ScholarPubMed
Gray, D., Gutierrez, C. & Cusick, C.G. (1996). Inferior pulvinar subdivisions in squirrel monkeys and macaques revealed by AChE histo-chemistry, Calbindin-D28K, Cat-301 immunostaining, and Wisteria floribunda agglutinin binding. Society for Neuroscience Abstracts 22, 399.Google Scholar
Gutierrez, C., Yaun, A. & Cusick, C.G. (1995). Neurochemical subdivisions of the inferior pulvinar in macaque monkeys. Journal of Comparative Neurology 363, 545–562.CrossRefGoogle ScholarPubMed
Harting, J.K., Huerta, M., Frankfurter, A.J., Strominger, N.L. & Royce, G.J. (1980). Ascending pathways from the monkey superior colliculus: An autoradiographic analysis. Journal of Comparative Neurology 192, 853–882.CrossRefGoogle ScholarPubMed
Hockfield, S., Mackay, R.D., Hendry, S.H.C. & Jones, E.G. (1983). 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 48, 877–889.CrossRefGoogle ScholarPubMed
Hollander, H. (1974). Projections from the striate cortex to the diencephalon in the squirrel monkey (Saimiri sciureus). A light microscopic radioautographic study following intracortical injections of H3 leucine. Journal of Comparative Neurology 155, 425–440.CrossRefGoogle Scholar
Jain, N., Preuss, T.M. & Kaas, J.H. (1994). Subdivisions of the visual system labeled with the Cat-301 antibody in tree shrew. Visual Neuroscience 11, 731–741.CrossRefGoogle Scholar
Jones, E.G. (1985). The Thalamus. New York and London: Plenum Press.CrossRefGoogle Scholar
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1972). Some principles of organization in the dorsal lateral geniculate nucleus. Brain, Behaviour, and Evolution 6, 253–299.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1982). The segregation of function in the nervous system: Why do sensory systems have so many subdivisions? In Contributions to Sensory Physiology, ed. Neff, W.P., pp. 201–240. New York: Academic Press.Google Scholar
Kaas, J.H. (1990). Processing areas and modules in sensory-perceptual cortex. In Signal and Sense: Local and Global order in Perceptual Maps, ed., Edelman, G.M., Gall, W.E. & Cowan, W.M., pp. 67–82. New York: John Wiley & Sons.Google Scholar
Kaas, J.H. & Krubitzer, L. A. (1992). Area 17 lesions deactivate area MT in owl monkeys. Visual Neuroscience 9, 399–408.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1996). Theories of visual cortex organization in primates: Areas of the third level. Progress in Brain Research 112, 213–221.CrossRefGoogle ScholarPubMed
Krubitzer, L. A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns. Visual Neuroscience 5, 165–204.CrossRefGoogle ScholarPubMed
Lin, C.-S., Wagor, E. & Kaas, J.H. (1974). Projections from the pulvinar to the middle temporal visual area (MT) in the owl monkey (Aotus trivirgatus). Brain Research 76, 145–149.CrossRefGoogle Scholar
Lin, C.-S. & Kaas, J.H. (1979). The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex. Journal of Comparative Neurology 187, 655–678.CrossRefGoogle ScholarPubMed
Lin, C.-S. & Kaas, J.H. (1980). Projections from the medial nucleus of the inferior pulvinar complex to the middle temporal area of the visual cortex. Neuroscience 5, 2219–2228.CrossRefGoogle Scholar
Lysakowski, A., Standage, G.P. & Benevento, L.A. (1986). Histochemical and architectonic differentiation of zones of pretectal and collicular inputs to the pulvinar and dorsal lateral geniculate nuclei in the macaque. Journal of Comparative Neurology 250, 431–448.CrossRefGoogle Scholar
Mathers, L.H. (1971). Tectal projection to the posterior thalamus of the squirrel monkey. Brain Research 35, 295–298.CrossRefGoogle Scholar
Maunsell, H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
Ogren, M.P. & Hendrickson, A.E. (1976). Pathways between striate cortex and subcortical regions in Macaca mulatta and Saimiri sciureus: Evidence for a reciprocal pulvinar connections. Experimental Neurology 53, 780–800.CrossRefGoogle Scholar
Partlow, G.D., Colonnier, M. & Szabo, J. (1977). Thalamic projections of the superior colliculus in the rhesus monkeey, Macaca mulatta. A light and electron microscopic study. Journal of Comparative Neurology 171, 285–318.CrossRefGoogle Scholar
Petersen, S.E., Robinson, D.L. & Keys, W. (1985). Pulvinar nuclei of the behaving rhesus monkey: Visual responses and their modulation. Journal of Neurophysiology 54, 867–886.CrossRefGoogle ScholarPubMed
Rausell, E. & Jones, E.G. (1991). Histochemical and immunocytochemical components of the VPM thalamic nucleus in monkeys project to different layers of somatosensory cortex. Journal of Neuroscience 11, 226–237.CrossRefGoogle ScholarPubMed
Rezak, M. & Benevento, L.A. (1979). A comparison of organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey. Brain Research 167, 19–40.CrossRefGoogle ScholarPubMed
Robinson, D.L. (1993). Functional contributions of the primate pulvinar. In Progress in Brain Research ed. Hicks, T.P., Molotchnikoff, S. & Ono, T., pp. 371–380. Amsterdam: Elsevier Science Publishers.Google Scholar
Rodman, H.R., Gross, C.G. & Albright, T.D. (1990). Afferent basis of visual response properties in area MT of the macaque: I. Effects of superior colliculus removal. Journal of Neuroscience 10, 1154–1164.CrossRefGoogle ScholarPubMed
Silito, A.M. & Kemp, J.A. (1983). Cholinergic modulation of the functional organization of the cat visual cortex. Brain Research 289, 143–155.CrossRefGoogle Scholar
Spatz, W.B. & TiGGES, J. (1973). Studies on the visual area MT in primates. II. Projection fibers to subcortical structures. Brain Research 61, 374–378.CrossRefGoogle ScholarPubMed
Standage, G.P. & Benevento, L.A. (1983). The organization of connections between the pulvinar and visual area MT in the macaque monkey. Brain Research 262, 288–294.CrossRefGoogle ScholarPubMed
Steele, G.E. & Weller, R.E. (1993). Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. Visual Neuroscience 10, 563–583.CrossRefGoogle ScholarPubMed
Stepniewska, I. & Kaas, J.H. (1995). Visuotopic organization of projections from the pulvinar complex to prestriate cortex (V2) in macaque monkeys. Acta Neurobiologiae Experimentalis (Suppl.) 55, 62.Google Scholar
Stepniewska, I. & Kaas, J.H. (1996). Architectonic subdivisions of the inferior pulvinar in New World and Old World monkeys. Society for Neuroscience Abstracts 22, 1817.Google Scholar
Stepniewska, I. & Kaas, J.H. Topographic patterns of V2 connections with the pulvinar in macaque monkeys (in preparation).Google Scholar
Symonds, L.L. & Kaas, J.H. (1978). Connections of striate cortex in the prosimian, Galago senegalensis. Journal of Comparative Neurology 181, 477–512.CrossRefGoogle ScholarPubMed
Ungerleider, L.G., Galkin, T.W. & Mishkin, M. (1983). Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey. Journal of Comparative Neurology 17, 137–157.CrossRefGoogle Scholar
Ungerleider, L.G., Desimone, R., Galkin, T.W. & Mishkin, M. (1984). Subcortical projections of area MT in the macaque. Journal of Comparative Neurology 223, 368–386.CrossRefGoogle ScholarPubMed
Wall, J.T., Symonds, L.L. & Kaas, J.H. (1982). Cortical and subcortical projections of the middle temporal area (MT) and adjacent cortex in galagos. Journal of Comparative Neurology 211, 193–214.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1977). Connections between the pulvinar nucleus and the prestriate cortex in the squirrel monkey as revealed by peroxidase histochemistry and autoradiography. Brain Research 134, 249–267.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, 11–29.CrossRefGoogle ScholarPubMed