Hostname: page-component-7dd5485656-c8zdz Total loading time: 0 Render date: 2025-10-29T20:06:00.828Z Has data issue: false hasContentIssue false
  • English
  • Français

Callosally projecting neurons in the macaque monkey V1/V2 border are enriched in nonphosphorylated neurofilament protein

Published online by Cambridge University Press:  02 June 2009

Patrick R. Hof ,
Leslie G. Ungerleider ,
Michelle M. Adams ,
Maree J. Webster ,
Ricardo Gattass ,
Dana M. Blumberg  and
John H. Morrison
Patrick R. Hof
Affiliation:
Neurobiology of Aging Laboratories and Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, New York Department of Geriatrics and Adult Development, Mount Sinai School of Medicine, New York Department of Ophthalmology, Mount Sinai School of Medicine, New York
Leslie G. Ungerleider
Affiliation:
Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda
Michelle M. Adams
Affiliation:
Neurobiology of Aging Laboratories and Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, New York Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda
Maree J. Webster
Affiliation:
Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda Slanley Foundation Research Program, National Institute of Mental Health Neuroscience Center at St. Elizabeth's, Washington D.C.
Ricardo Gattass
Affiliation:
Departamento de Neurobiologia, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941–900, Brasil
Dana M. Blumberg
Affiliation:
Neurobiology of Aging Laboratories and Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, New York
John H. Morrison
Affiliation:
Neurobiology of Aging Laboratories and Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, New York Department of Geriatrics and Adult Development, Mount Sinai School of Medicine, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

Previous immunohistochemical studies combined with retrograde tracing in macaque monkeys have demonstrated that corticocortical projections can be differentiated by their content of neurofilament protein. The present study analyzed the distribution of nonphosphorylated neurofilament protein in callosally projecting neurons located at the V1/V2 border. All of the retrogradely labeled neurons were located in layer III at the V1/V2 border and at an immediately adjacent zone of area V2. A quantitative analysis showed that the vast majority (almost 95%) of these interhemispheric projection neurons contain neurofilament protein immunoreactivity. This observation differs from data obtained in other sets of callosal connections, including homotypical interhemispheric projections in the prefrontal, temporal, and parietal association cortices, that were found to contain uniformly low proportions of neurofilament protein-immunoreactive neurons. Comparably, highly variable proportions of neurofilament protein-containing neurons have been reported in intrahemispheric corticocortical pathways, including feedforward and feedback visual connections. These results indicate that neurofilament protein is a prominent neurochemical feature that identifies a particular population of interhemispheric projection neurons at the V1/V2 border, and suggest that this biochemical attribute may be critical for the function of this subset of callosal neurons.

Keywords

Callosal projectionsCytoskeletonNeurochemical codingNeurofilament proteinPrimate visual system

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 981 - 987
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Antonini, A., Berlucchi, G. & Lepore, F. (1983). Physiological organization of callosal connections of a visual lateral suprasylvian cortical area in the cat. Journal of Neurophysiology 49, 902–921.CrossRefGoogle ScholarPubMed
Berlucchi, G. & Rizzolatti, G. (1968). Binocularly driven neurons in visual cortex of split chiasm cats. Science 159, 308–310.CrossRefGoogle ScholarPubMed
Blakemore, C., Diao, Y., Pu, M., Wang, Y. & Xiao, Y. (1983). Possible function of the interhemispheric connexions between visual cortical areas in the cat. Journal of Physiology (London) 337, 334–349.CrossRefGoogle ScholarPubMed
Bloom, F.E., Young, W.G., Nimchinsky, E.A., Hof, P.R. & Morrison, J.H. (1997). Neuronal vulnerability and informatics in human disease. In Progress in Neuroinformatics Research, Vol. I, Neuroinformatics—An Overview of the Human Brain Project, ed. Koslow, S.H. & Huerta, M.F., pp. 83–123. Mahwah, N.J.: Lawrence Erlbaum.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., Hof, P.R. & Morrison, J.H. (1991). A subpopulation of primate corticocortical neurons is distinguished by somatodendritic distribution of neurofilament protein. Brain Research 539, 133–136.CrossRefGoogle ScholarPubMed
Chaudhuri, A., Zangenehpour, S., Matsubara, J.A. & Cynader, M.S. (1996). Differential expression of neurofilament protein in the visual system of the vervet monkey. Brain Research 709, 17–26.CrossRefGoogle ScholarPubMed
Choudhury, B.P., Whitteridge, D. & Wilson, M.E. (1965). The function of the callosal connections of the visual cortex. Quarterly Journal of Experimental Physiology 50, 214–219.CrossRefGoogle ScholarPubMed
De Lima, A.D., Voigt, T. & Morrison, J.H. (1990). Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey. Journal of Comparative Neurology 296, 159–272.CrossRefGoogle Scholar
Desimone, R., Moran, J., Schein, S.J. & Mishkin, M. (1993). A role for the corpus callosum in visual area V4 of the macaque. Visual Neuroscience 10, 158–171.CrossRefGoogle ScholarPubMed
Glickstein, M. & Whitteridge, D. (1976). Degeneration of layer III pyramidal cells in area 18 following destruction of callosal input. Brain Research 104, 148–151.CrossRefGoogle ScholarPubMed
Gould, H.J. III, Weber, J.T. & Rieck, R.W. (1987). Interhemispheric connections in the visual cortex of the squirrel monkey (Saimiri sciureus). Journal of Comparative Neurology 265, 14–28.CrossRefGoogle Scholar
Harvey, A.R. (1980). A physiological analysis of subcortical and commissural projections of areas 17 and 18 of the cat. Journal of Physiology (London) 302, 507–534.CrossRefGoogle ScholarPubMed
Hof, P.R. & Morrison, J.H. (1995). Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. Journal of Comparative Neurology 352, 161–186.CrossRefGoogle ScholarPubMed
Hof, P.R., Nimchinsky, E.A. & Morrison, J.H. (1995 a). Neurochemical phenotype of corticocortical connections in the macaque monkey: Quantitative analysis of a subset of neurofilament protein-immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices. Journal of Comparative Neurology 362, 109–133.CrossRefGoogle ScholarPubMed
Hof, P.R., Ungerleider, L.G., Webster, M.J., Gattass, R., Adams, M.M., Sailstad, C.A., Janssen, W.G.M. & Morrison, J.H. (1995 b). Feed-forward and feedback corticocortical projections in the monkey visual system display differential neurochemical phenotype. Society for Neuroscience Abstracts 21, 904.Google Scholar
Hof, P.R., Ungerleider, L.G., Webster, M.J., Gattass, R., Adams, M.M., Sailstad, C.A. & Morrison, J.H. (1996). Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. Journal of Comparative Neurology 376, 112–127.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Hoffman, P.N., Cleveland, D.W., Griffin, J.W., Landes, P.W., Cowan, N.J. & Price, D.L. (1987). Neurofilament gene expression: A major determinant of axonal caliber. Proceedings of the National Academy of Sciences of the U.S.A. 84, 3472–3476.CrossRefGoogle Scholar
Houzel, J.C., Milleret, C. & Innocenti, G. (1994). Morphology of callosal axons interconnecting areas 17 and 18 of the cat. European Journal of Neuroscience 6, 898–917.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1967). Cortical and callosal projections concerned with the vertical meridian of vertical visual fields in the cat. Journal of Neurophysiology 30, 1561–1573.CrossRefGoogle Scholar
Innocenti, G.M. (1986). General organization of callosal connections in the cerebral cortex. In Cerebral Cortex, Vol. 5, Sensory-Motor Areas and Aspects of Cortical Connectivity, ed. Jones, E.G. & Peters, A., pp. 291–355. New York: Plenum Press.Google Scholar
Innocenti, G.M., Lehmann, P. & Houzel, J.C. (1994). Computational structure of visual callosal axons. European Journal of Neuroscience 6, 918–935.CrossRefGoogle ScholarPubMed
Kennedy, H., Dehay, C. & Bullier, J. (1986). Organization of the callosal connections of visual areas VI and V2 in the macaque monkey. Journal of Comparative Neurology 247, 398–415.CrossRefGoogle Scholar
Land, E.H., Hubel, D.H., Livingstone, M.S., Perry, S.H. & Burns, M.M. (1983). Colour-generating interactions across the corpus callosum. Nature 303, 616–618.CrossRefGoogle ScholarPubMed
Lawson, S.N. & Waddell, J.P. (1991). Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. Journal of Physiology (London) 435, 41–63.CrossRefGoogle ScholarPubMed
Lee, V.M.Y., Otvos, L. Jr, Carden, M.J., Hollosi, M., Dietzschold, B. & Lazzarini, R.A. (1988). Identification of the major multiphosphorylation site in mammalian neurofilaments. Proceedings of the National Academy of Sciences of the U.S.A. 85, 1998–2002.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
Maunsell, J.H.R. & Van Essen, D.C. (1987). Topographic organization of middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries. Journal of Comparative Neurology 266, 535–555.CrossRefGoogle ScholarPubMed
Meissirel, C., Dehay, C., Berland, M. & Kennedy, H. (1991). Segregation of callosal and association pathways during development in the visual cortex of the primate. Journal of Neuroscience 11, 3297–3316.CrossRefGoogle ScholarPubMed
Morris, J.R. & Laser, R.J. (1982). Stable polymers of the axonal cytoskeleton: The axoplasmic ghost. Journal of Cell Biology 92, 192–198.CrossRefGoogle ScholarPubMed
Myers, R.E. (1962). Commissural connections between occipital lobes of the monkey. Journal of Comparative Neurology 118, 1–10.CrossRefGoogle ScholarPubMed
Nimchinsky, E.A., Hof, P.R., Young, W.G. & Morrison, J.H. (1996). Neurochemical, morphologic and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey. Journal of Comparative Neurology 374, 136–160.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Nixon, R.A., Paskevich, P.A., Sihag, R.K. & Thayer, C.Y. (1994). Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: Influences on regional neurofilament accumulation, interneuronal spacing, and axonal caliber. Journal of Cell Biology 126, 1031–1046.CrossRefGoogle Scholar
Olavarria, J.F. (1996). Non-mirror–symmetric patterns of callosal linkages in areas 17 and 18 in cat visual cortex. Journal of Comparative Neurology 366, 643–655.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Olavarria, J.F. & Abel, P.F. (1996). The distribution of callosal connections correlates with the pattern of cytochrome oxidase stripes in visual area V2 of macaque monkeys. Cerebral Conex 6, 631–639.CrossRefGoogle ScholarPubMed
Pandya, D.N., Karol, E.A. & Heilbrom, D. (1971). The topographic distribution of interhemispheric projections in the corpus callosum of the rhesus monkey. Brain Research 32, 31–43.CrossRefGoogle ScholarPubMed
Payne, B.R. (1990). Representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex. Visual Neuroscience 4, 445–474.CrossRefGoogle ScholarPubMed
Payne, B.R. (1994). Neuronal interactions in cat visual cortex mediated by the corpus callosum. Behavioural Brain Research 64, 55–64.CrossRefGoogle ScholarPubMed
Pijak, D.S., Hall, G.F., Tenicki, P.J., Boulos, A.S., Lurie, D.I. & Selzer, M.S. (1996). Neurofilament spacing, phosphorylation, and axon diameter in regenerating and uninjured lamprey axons. Journal of Comparative Neurology 368, 569–581.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Riederer, B.M., Draberova, E., Viklicky, V. & Draber, P. (1995). Changes of MAP2 phosphorylation during brain development. Journal of Histochemistry and Cytochemistry 43, 1269–1284.CrossRefGoogle ScholarPubMed
Riederer, B.M., Porchet, R. & Marugg, R.A. (1996). Differential expression and modification of neurofilament triplet proteins during cat cerebellar development. Journal of Comparative Neurology 364, 704–717.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Rockland, K.S. (1989). Bistratified distribution of terminal arbors of individual axons projecting from area VI to middle temporal area (MT) in the macaque monkey. Visual Neuroscience 3, 155–170.CrossRefGoogle Scholar
Rockland, K.S. (1995). Morphology of individual axons projecting from area V2 to MT in the macaque. Journal of Comparative Neurology 355, 15–26.CrossRefGoogle Scholar
Spatz, W.B. & Kunz, B. (1984). Area 17 of anthropoid primates does participate in visual callosal connections. Neuroscience Letters 48, 49–53.CrossRefGoogle ScholarPubMed
Spatz, W.B., Kunz, B. & Steffen, H. (1987). A new heterotopic callosal projection of primary visual cortex in the monkey, Callithrix jacchus. Brain Research 403, 158–161.CrossRefGoogle ScholarPubMed
Sternberger, L.A. & Sternberger, N. (1983). Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proceedings of the National Academy of Sciences of the U.S.A. 80, 6126–6130.CrossRefGoogle ScholarPubMed
Toyama, K., Matsunami, K. & Ohno, T. (1969). Antidromic identification of association, commissural and corticofugal efferent cells in cat visual cortex. Brain Research 14, 513–517.CrossRefGoogle ScholarPubMed
Van Essen, D.C., Newsome, W.T. & Bixby, J.L. (1982). The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey. Journal of Neuroscience 2, 265–283.CrossRefGoogle ScholarPubMed
Vercelli, A. & Innocenti, G.M. (1993). Morphology of visual callosal neurons with different locations, contralateral targets or patterns of development. Experimental Brain Research 94, 393–404.CrossRefGoogle ScholarPubMed
Vercelli, A., Assal, F. & Innocenti, G.M. (1992). Emergence of callosally projecting neurons with stellate morphology in the visual cortex of the kitten. Experimental Brain Research 90, 346–358.CrossRefGoogle ScholarPubMed
Voigt, T., LeVay, S. & Stamnes, M.A. (1988). Morphological and immunocytochemical observations on the visual callosal projections in the cat. Journal of Comparative Neurology 272, 450–460.CrossRefGoogle ScholarPubMed
Von Economo, C. (1927). L'Architecture Cellulaire Normale de l'Écorce Cérébrate. Paris: Masson.Google Scholar
Weisskopf, M. & Innocenti, G.M. (1991). Neurons with callosal projections in visual areas of newborn kittens: An analysis of their dendritic phenotype with respect to the fate of the callosal axon and of its target. Experimental Brain Research 86, 151–158.CrossRefGoogle Scholar
Xu, Z., Marszalek, J.R., Lee, M.K., Wong, P.C., Folmer, J., Crawford, T.O., Hsieh, S.T., Griffin, J.W. & Cleveland, D.W. (1996). Subunit composition of neurofilaments specifies axonal diameter. Journal of Cell Biology 133, 1061–1069.CrossRefGoogle ScholarPubMed
Young, W.G., Morrison, J.H., Hof, P.R., Nimchinsky, E.A. & Bloom, F.E. (1996). NeuroZoom—Topographical mapping and stereological counting, distribution of data, and collaborative computing. Society for Neuroscience Abstracts 22, 1238.Google Scholar
Zeki, S.M. (1970). Interhemispheric connections of prestriate cortex in monkey. Brain Research 19, 63–75.CrossRefGoogle ScholarPubMed