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Calcium-binding proteins immunoreactivity in the human subcortical and cortical visual structures

Published online by Cambridge University Press:  02 June 2009

G. Leuba  and
K. Saini
G. Leuba
Affiliation:
University Psychogeriatrics Hospital, CH-1008 Lausanne-Prilly, Switzerland
K. Saini
Affiliation:
University Psychogeriatrics Hospital, CH-1008 Lausanne-Prilly, Switzerland
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Abstract

The distribution of neurons and fibers immunoreactive (ir) to the three calcium-binding proteins parvalbumin (PV), calbindin D-28k (CB), and calretinin (CR) was studied in the human lateral geniculate nucleus (LGN), lateral inferior pulvinar, and optic radiation, and related to that in the visual cortex. In the LGN, PV, CR, and CB immunoreactivity was present in all laminae, slightly stronger in the magnocellular than in the parvocellular laminae for CB and CR. PV-ir puncta, representing transversally cut axons, and CR-ir fibers were revealed within the laminae and interlaminar zones, and just beyond the outer border of lamina 6 in the geniculate capsule. In the optic radiation both PV- and CR-immunoreactive neurons, puncta, and fibers were present. CB immunoreactivity was revealed in neurons of all laminae of the lateral geniculate nucleus, including S lamina and interlaminar zones. There were hardly any CB-ir puncta or fibers in the laminae, interlaminar zones, geniculate capsule, or optic radiation. In the lateral inferior pulvinar, immunoreactive neurons for the three calcium-binding proteins were present in smaller number than in the LGN, as well as PV-ir puncta and CR-ir fibers within the nucleus and in the pulvinar capsule. In the white matter underlying area 17, fibers intermingled with a few scattered neurons were stained for both PV and CR, but very rarely for CB. These fibers stopped at the limit between areas 17 and 18. Area 17 showed a dense plexus of PV-ir puncta and neurons in the thalamo-receptive layer IV and CR-ir puncta and neurons both in the superficial layers I-II, IIIC, and in layer VA. Cajal-Retzius CR-ir neurons were present in layer I. CB-ir puncta were almost confined to layer I-III and CB-ir neurons to layer II. Finally the superior colliculus exhibited mostly populations of PV and CR pyramidal-like immunoreactive neurons, mainly in the intermediate tier. These data suggest that in the visual thalamus most calcium-binding protein immunoreactive neurons project to the visual cortex, while in the superior colliculus a smaller immunoreactive population represent projection neurons.

Keywords

Calcium-binding proteinsLateral geniculate nucleusVisual cortexSuperior colliculusHuman
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 997 - 1009
Copyright
Copyright © Cambridge University Press 1996

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References

Arai, M., Arai, R., Kani, K. & Jacobowitz, D.M. (1992). Immunohistochemical localization of calretinin in the rat lateral geniculate nucleus and its retino-geniculate projection. Brain Research 596, 215–222.CrossRefGoogle ScholarPubMed
Baimbridge, K.G., Celio, M.R. & Rogers, J.H. (1992). Calcium-binding proteins in the nervous system. Trends in Neurosciences 15, 303–308.Google Scholar
Baizer, J.S., Desimone, R. & Ungerleider, L.G. (1993). Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys. Visual Neuroscience 10, 59–72.CrossRefGoogle ScholarPubMed
Belichenko, P.V., Vogt, Weisenhorn D.M., Myklossy, J. & Celio, M.R. (1995). Calretinin-positive Cajal-Retzius cells persist in the adult human neocortex. Neuroreport 6, 1869–1874.Google 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
Blümcke, I., Hof, P.R., Morrison, J.H. & Celio, M.R. (1991). Parvalbumin in the monkey striate cortex: A quantitative immunoelectron-microscopy study. Brain Research 554, 237–243.Google Scholar
Blümcke, I., Weruaga, E., Kasas, S., Hendrickson, A.E. & Celio, M.R. (1994). Discrete reduction patterns of parvalbumin and cal-bindin D-28k immunoreactivity in the dorsal lateral geniculate nucleus and the striate cortex of adult macaque monkeys after monocular enucleation. Visual Neuroscience 11, 1–11.CrossRefGoogle Scholar
Blümcke, I. & Celio, M.R. (1992). Parvalbumin and calbindin D-28k immunoreactivities coexist within cytochrome oxidase-rich compartments of squirrel monkey area 18. Experimental Brain Research 92, 39–45.Google Scholar
Braak, H. & Bachmann, A. (1985). The percentage of projection neurons and interneurons in the human lateral geniculate nucleus. Human Neurobiology 4, 91–95.Google Scholar
Casacrande, V.A. (1994). A third parallel visual pathway to primate area VI. Trends in Neurosciences 17, 305–310.Google Scholar
Casagrande, V.A. & Norton, T.T. (1991). Lateral geniculate nucleus: A review of its physiology and function. In Vision and Visual Dysfunction, Vol. 4, The Neural Basis of Visual function, ed. Leventhal, E. & Cronley-Dillon, J.R., pp. 41–84. London: Macmillan Press.Google Scholar
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.Google Scholar
DeFelipe, J. & Jones, E.G. (1991). Parvalbumin immunoreactivity reveals layer IV of monkey cerebral cortex as a mosaic of microzones of thalamic afferent terminations. Brain Research 362, 39–47.Google Scholar
Diamond, I.T., Fitzpatrick, D. & Schmechel, D. (1993). Calciumbinding proteins distinguish large and small cells of the ventral posterior and lateral geniculate nuclei of the prosimian galago and the tree shrew (Tupaia belanger). Proceedings of the National Academy of Sciences of the U.S.A. 90, 1425–1429.Google Scholar
Eckert, A., Hartmann, H., Forstl, H. & Muller, W.E. (1994). Alterations of imracellular calcium regulation during aging and Alzheimer's disease in nonneuronal cells. Life Sciences 55, 2019–2029.Google Scholar
Fonseca, M., Soriano, E., Ferrer, I., Martinez, A. & Tunon, T. (1993). Chandelier cell axons identified by parvalbumin-immunore-activity in the normal human temporal cortex and in Alzheimer's disease. Neuroscience 55, 1107–1116.Google Scholar
Ghosh, A. & Shatz, C.J. (1992). Pathfinding and target selection by developing geniculocortical axons. Journal of Neuroscience 12, 39–55.Google Scholar
Glezer, I.I., Hof, P.R. & Morgane, P.J. (1992). Calretinin-immunore-active neurons in the primary visual cortex of dolphin and human brains. Brain Research 595, 181–188.Google Scholar
Gutierrez, C. & Cusick, C.G. (1994). Effects of chronic monocular enucleation on calcium binding proteins calbindin-D28k and parvalbumin in the lateral geniculate nucleus of adult rhesus monkeys. Brain Research 651, 300–310.Google Scholar
Hashikawa, T., Rausell, E., Molinari, M. & Jones, E.G. (1991). Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: Differential distributions and cortical layer specific projections. Brain Research 544, 335–341.Google Scholar
Heizmann, C.W. (1992). Calcium-binding proteins: Basic concepts and clinical implications. General Physiology and Biophysics 11, 411–425.Google Scholar
Heizmann, C.W. (1993). Calcium signaling in the brain. Acta Neuro-biologiae Experimentalis 53, 15–23.Google Scholar
Heizmann, C.W. & Braun, K. (1992). Changes in Ca2+-binding proteins in human neurodegenerative disorders. Trends in Neurosciences 15, 259–264.Google Scholar
Hendry, S.H.C. & Carder, R.K. (1993). Neurochemical compart-mentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species. Visual Neuroscience 10, 1109–1120.Google Scholar
Hockfield, S., Tootell, R.B. & 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.Google Scholar
Hockfield, S. & Sur, M. (1990). Monoclonal antibody Cat-301 identifies Y-cells in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 300, 320–330.Google Scholar
Jacobowitz, D.M. & Winsky, L. (1991). Immunocytochemical localization of calretinin in the forebrain of the rat. Journal of Comparative Neurology 304, 198–218.Google Scholar
Johnson, J.K. & Casagrande, V.A. (1995). Distribution of calcium-binding proteins within the parallel visual pathways of a primate (Galago crassicaudatus). Journal of Comparative Neurology 356, 238–260.CrossRefGoogle ScholarPubMed
Jones, E.G. (1993). GABAergic neurons and their role in cortical plasticity in primates. Cerebral Cortex 3, 361–372.Google Scholar
Jones, E.G. & Hendry, S.H.C. (1989). Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. European Journal of Neuroscience 1, 222–246.Google Scholar
Lachica, E.A. & Casagrande, V.A. (1993). The morphology of col-licular and retinal axons ending on small relay (W-like) cells of the primate lateral geniculate nucleus. Visual Neuroscience 10, 403–418.Google Scholar
Leichnetz, G.R. (1990). Preoccipital cortex receives a differential input from the frontal eye field and projects to the pretectal olivary nucleus and other visuomotor-related structures in the rhesus monkey. Visual Neuroscience 5, 123–133.Google Scholar
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.Google Scholar
Ma, T.P., Cheng, H.-W., Czech, J.A. & Rafols, J.A. (1990). Intermediate and deep layers of the macaque superior colliculus: A Golgi study. Journal of Comparative Neurology 295, 92–110.CrossRefGoogle ScholarPubMed
Maioli, M., Galletti, C., Squatrito, S., Battaglini, P.P. & Riva, Sanseverino E. (1984). Projections from the cortex of the superior temporal sulcus to the dorsal lateral geniculate and pregeniculate nuclei in the macaque monkey. Archives italiennes de Biologie 122, 301–309.Google Scholar
Mize, R.R., Luo, Q., Butler, G., Jeon, C.-J. & Nabors, B. (1992 a). The calcium binding proteins parvalbumin and calbindin-D 28K form complementary patterns in the cat superior colliculus. Journal of Comparative Neurology 320, 243–256.Google Scholar
Mize, R.R., Luo, Q. & Tigges, M. (1992 b). Monocular enucleation reduces immunoreactivity to the calcium-binding protein calbindin 28kD in the Rhesus monkey lateral geniculate nucleus. Visual Neuroscience 9, 471–482.Google Scholar
Mize, R.R. & Hockfield, S. (1989). Cat-301 antibody selectively labels neurons in the Y-innervated laminae of the cat superior colliculus. Visual Neuroscience 3, 433–443.Google ScholarPubMed
Mize, R.R. & Luo, Q. (1992). Visual deprivation fails to reduce calbindin 28kD or GABA immunoreactivity in the Rhesus monkey superior colliculus. Visual Neuroscience 9, 157–168.Google Scholar
Moore, R.Y. (1993). Organization of the primate circadian system. Review. Journal of Biological Rhythms 8 (Suppl.) S3–S9.Google Scholar
Morecraft, R.J., Geula, C. & Mesulam, M.M. (1992). Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. Journal of Comparative Neurology 323, 341–358.Google Scholar
Mustari, M.J., Fuchs, A.F., Kaneko, C.R. & Robinson, F.R. (1994). Anatomical connections of the primate pretectal nucleus of the optic tract. Journal of Comparative Neurology 349, 111–128.Google Scholar
Pasteels, B., Rogers, J., Blacker, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.Google Scholar
Rausell, E. & Jones, E.G. (1991). Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representation map. Journal of Neuroscience 11, 210–225.Google Scholar
Stein, B.E. & Meredith, M.E. (1993). Anatomical organization of the superior colliculus. In The Merging of the Senses, ed. Gazzaniga, M.S., pp. 41–49. Cambridge, London: A Bradford Book, The MIT Press.Google Scholar
Stichel, C.C., Singer, W. & Heizmann, C.W. (1988). Light and electron immunocytochemical localization of parvalbumin in the dorsal geniculate nucleus of the cat: Evidence for coexistence with GABA. Journal of Comparative Neurology 268, 29–37.Google Scholar
Tigges, M. & Tigges, J. (1993). Parvalbumin immunoreactivity in the lateral geniculate nucleus of rhesus monkeys raised under monocular and binocular deprivation conditions. Visual Neuroscience 10, 1043–1053.Google Scholar
Tunon, T., Insausti, R., Ferrer, I., Sobreviela, T. & Soriano, E. (1992). Parvalbumin and calbindin D-28K in the human entorhinal cortex. An immunohistochemical study. Brain Research 589, 24–31.Google Scholar