Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-29T02:32:43.646Z Has data issue: false hasContentIssue false
  • English
  • Français

Topographic organization, number, and laminar distribution of callosal cells connecting visual cortical areas 17 and 18 of normally pigmented and Siamese cats

Published online by Cambridge University Press:  02 June 2009

Nancy E. J. Berman  and
Simon Grant
Nancy E. J. Berman
Affiliation:
Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City
Simon Grant
Affiliation:
Department of Anatomy, Medical College of Pennsylvania, Philadelphia
Get access Rights & Permissions [Opens in a new window]

Abstract

The callosal connections between visual cortical areas 17 and 18 in adult normally pigmented and “Boston” Siamese cats were studied using degeneration methods, and by transport of WGA-HRP combined with electrophysiological mapping. In normal cats, over 90% of callosal neurons were located in the supragranular layers. The supragranular callosal cell zone spanned the area 17/18 border and extended, on average, some 2–3 mm into both areas to occupy a territory which was roughly co-extensive with the distribution of callosal terminations in these areas. The region of the visual field adjoining the vertical meridian that was represented by neurons in the supragranular callosal cell zone was shown to increase systematically with decreasing visual elevation. Thus, close to the area centralis, receptive-field centers recorded from within this zone extended only up to 5 deg into the contralateral hemifield but at elevations of -10 deg and -40 deg they extended as far as 8 deg and 14 deg, respectively, into this hemifield. This suggests an element of visual non-correspondence in the callosal pathway between these cortical areas, which may be an essential substrate for “coarse” stereopsis at the visual midline.

In the Siamese cats, the callosal cell and termination zones in areas 17 and 18 were expanded in width compared to the normal animals, but the major components were less robust. The area 17/18 border was often devoid of callosal axons and, in particular, the number of supragranular layer neurons participating in the pathway were drastically reduced, to only about 25% of those found in the normally pigmented adults. The callosal zones contained representations of the contralateral and ipsilateral hemifields that were roughly mirror-symmetric about the vertical meridian, and both hemifield representations increased with decreasing visual elevation. The extent and severity of the anomalies observed were similar across individual cats, regardless of whether a strabismus was also present. The callosal pathway between these visual cortical areas in the Siamese cat has been considered “silent,” since nearly all neurons within its territory are activated only by the contralateral eye. The paucity of supragranular pyramidal neurons involved in the pathway may explain this silence.

Keywords

Corpus callosumCerebral cortexAlbinism
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 1 , July 1992 , pp. 1 - 19
Copyright
Copyright © Cambridge University Press 1992

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.)

References

Albus, K. (1975). A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. I. The precision of the topography. Experimental Brain Research 24, 159–179.CrossRefGoogle ScholarPubMed
Berlucchi, G., Gazzaniga, M.S. & Rizzolatti, G. (1967). Microelectrode analysis of transfer of visual information by the corpus callosum. Archives of Italian Biology 105, 583–596.Google ScholarPubMed
Berlucchi, G. & Rizzolatti, G. (1968). Binocularly driven neurons in visual cortex of split-chiasm cats. Science 159, 308–310.CrossRefGoogle ScholarPubMed
Berman, N. & Payne, B.R. (1983). Alterations in connections of the corpus callosum following convergent and divergent strabismus. Brain Research 274, 201–212.CrossRefGoogle ScholarPubMed
Berman, N., Payne, B.R., Labar, D. & Murphy, E.H. (1982). Functional organization of cat striate cortex: Variations in ocular dominance and receptive field type with cortical laminae and location in the visual field. Journal of Neurophysiology 48, 1051–1072.CrossRefGoogle ScholarPubMed
Bishop, P.O. & Henry, G.H. (1971). Spatial vision. Annual Review of Psychology 22, 119–160.CrossRefGoogle ScholarPubMed
Blakemore, C. (1969). Binocular depth discrimination and the nasotemporal division. Journal of Physiology (London) 205, 471–497.CrossRefGoogle ScholarPubMed
Blakemore, C. (1970). Binocular depth perception and the optic chiasm. Vision Research 10, 43–47.CrossRefGoogle ScholarPubMed
Blakemore, C., Diao, Y., Pu, M.L., Wang, Y. & Xiao, Y. (1983). Possible functions of the interhemispheric connections between visual cortical areas in the cat. Journal of Physiology (London) 337, 331–349.CrossRefGoogle ScholarPubMed
Buhl, E.H. & Singer, W. (1989). The callosal projection in cat visual cortex as revealed by a combination of retrograde tracing and intra-cellular injection. Experimental Brain Research 75, 470–476.CrossRefGoogle Scholar
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
Clare, M.H., Landau, W.M. & Bishop, G.H. (1961). The cortical response to direct stimulation of the corpus callosum in the cat. Electroencephalography and Clinical Neurophysiology 13, 21–33.CrossRefGoogle ScholarPubMed
Cooper, M.L. & Blasdel, G.G. (1980). Regional variation in the representation of the visual field in the visual cortex of the Siamese cat. Journal of Comparative Neurology 193, 237–253.CrossRefGoogle ScholarPubMed
Diao, Y.-C., Jia, W.-G., Swindale, N.V. & Cynader, M.S. (1990). Functional organization of the cortical 17/18 border region in the cat. Experimental Brain Research 79, 271–282.CrossRefGoogle ScholarPubMed
Ebner, F.F. & Myers, R.E. (1965). Distribution of corpus callosum and anterior commissure in cat and raccoon. Journal of Comparative Neurology 124, 353–366.CrossRefGoogle Scholar
Elberger, A. (1989). Selective labeling of visual corpus callosum connections with aspartate in cat and rat. Visual Neuroscience 2, 81–85.CrossRefGoogle Scholar
Gardner, J.C. & Cynader, M.S. (1987). Mechanisms for binocular depth sensitivity along the vertical meridian of the visual field. Brain Research 413, 60–74.CrossRefGoogle ScholarPubMed
Garey, L.J., Jones, E.G., & Powell, T.P.S. (1968). Interrelationships of striate and extrastriate cortex with the primary relay sites of the visual pathway. Journal of Neurology and Neurosurgical Psychiatry 31, 135–157.CrossRefGoogle ScholarPubMed
Grant, S. & Berman, N.E.J. (1992). Development of visual callosal connections in normally pigmented and Siamese cats. Visual Neuroscience (submitted).Google Scholar
Guillery, R.W. & Kaas, J. (1971). A study of normal and congenitally abnormal retinogeniculate projections in cats. Journal of Comparative Neurology 143, 73–100.CrossRefGoogle ScholarPubMed
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
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106–154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1967). Cortical and callosal connections concerned with the vertical meridian of the visual fields in the cat. Journal of Neurophysiology 30, 1561–1573.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1971). Aberrant visual projections in the Siamese cat. Journal of Physiology (London) 218, 33–62.CrossRefGoogle ScholarPubMed
Innocenti, G.M. (1980). The primary visual pathway through the corpus callosum; morphological and functional aspects in the cat. Archives of Italian Biology 118, 124–188.Google ScholarPubMed
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. 291–354. New York: Plenum Press.Google Scholar
Innocenti, G.M. & Fiore, L. (1976). Morphological correlates of visual field transformation in the corpus callosum. Neuroscience Letters 2, 245–252.CrossRefGoogle ScholarPubMed
Innocenti, G.M. & Frost, D.O. (1979). Effects of visual experience on the maturation of the efferent system to the corpus callosum. Nature 280, 231–234.CrossRefGoogle ScholarPubMed
Innocenti, G.M., Frost, D.O. & Illes, J. (1985). Maturation of visual callosal connections in visually deprived kittens: A challenging critical period. Journal of Neuroscience 5, 225–267.CrossRefGoogle ScholarPubMed
Jones, E.G., Coulter, J.D. & Wise, S.P. (1979). Commissural columns in the sensory-motor cortex of monkeys. Journal of Comparative Neurology 188, 113–136.CrossRefGoogle ScholarPubMed
Keller, G. & Innocenti, G.M. (1981). Callosal connections of suprasylvian visual areas in the cat. Neuroscience 6, 703–712.CrossRefGoogle ScholarPubMed
Konigsmark, B.W. (1970). Methods for the counting of neurons. In Contemporary Research Methods in Neuroanatomy, ed. Nauta, W.J.H., & Ebesson, S.O.E. pp. 315–340. New York: Springer.CrossRefGoogle Scholar
Leicester, J. (1968). Projection of the visual vertical meridian to cerebral cortex of the cat. Journal of Neurophysiology 31, 371–382.CrossRefGoogle ScholarPubMed
Lepore, F. & Guillemot, J.-P. (1982). Visual receptive field properties of cells innervated through the corpus callosum in the cat. Experimental Brain Research 46, 413–424.CrossRefGoogle ScholarPubMed
Lepore, F., Ptito, M. & Lassonde, M. (1986). Stereoperception in cats following section of the corpus callosum and/or the optic chiasma. Experimental Brain Research 61, 258–264.CrossRefGoogle ScholarPubMed
Lund, R.D., Mitchell, D.E. & Henry, G.H. (1978). Squint-induced modification of callosal connections in cats. Brain Research 144, 169–172.CrossRefGoogle ScholarPubMed
Manzoni, T., Barbaresi, P., Conti, F. & Fabri, M. (1989). The callosal connections of the primary somatosensory cortex and the neural bases of midline fusion. Experimental Brain Research 76, 251–266.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1982). Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways. Axonal transport, enzyme histochemistry and light microscopic analysis. In Tracing Neural Connections with Horseradish Peroxidase, ed. Mesulam, M.-M., pp. 1–152. New York: Wiley.Google Scholar
Mitchell, D.E. (1969). Qualitative depth localization with diplopic images of dissimilar shape. Vision Research 9, 991–994.CrossRefGoogle ScholarPubMed
Mitchell, D.E. (1970). Properties of stimuli eliciting vergence eye movements and stereopsis. Vision Research 10, 145–162.CrossRefGoogle ScholarPubMed
Mitchell, D.E. & Blakemore, C. (1970). Binocular depth perception and the corpus callosum. Vision Research 10, 49–54.CrossRefGoogle ScholarPubMed
Packwood, J. & Gordon, B. (1975). Stereopsis in normal domestic cat, Siamese cat, and cat raised with alternating monocular occlusion. Journal of Neurophysiology 3, 1485–1499.CrossRefGoogle Scholar
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., Berman, N. & Murphy, E.H. (1981). A quantitative assessment of eye alignment after corpus callosum transection. Experimental Brain Research 43, 371–376.Google ScholarPubMed
Payne, B.R., Elberger, A.J., Berman, N. & Murphy, E.H. (1980). Binocularity in cat visual cortex is reduced by corpus callosum section. Science 207, 1097–1099.CrossRefGoogle Scholar
Payne, B.R., Pearson, H.E. & Berman, N. (1984). Role of the corpus callosum in functional organization of cat striate cortex. Journal of Neurophysiology 52, 570–594.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google ScholarPubMed
Sanides, D. & Albus, K. (1980). The distribution of interhemispheric projections in area 18 of the cat: Coincidence with discontinuities of the representation of the visual field in the second visual area (V2). Experimental Brain Research 38, 237–240.CrossRefGoogle ScholarPubMed
Segraves, M.A. & Rosenquist, A.C. (1982a). The distribution of cells of origin of callosal projections in cat visual cortex. Journal of Neuroscience 2, 1079–1089.CrossRefGoogle ScholarPubMed
Segraves, M.A. & Rosenquist, A.C. (1982b). The afferent and efferent callosal connections of retinotopically defined areas in cat cortex. Journal of Neuroscience 2, 1090–1107.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1977a). A comparison of visual pathways in Boston and Midwestern Siamese cats. Journal of Comparative Neurology 171, 205–228.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1977b). Abnormal interhemispheric connections in the visual system of Boston Siamese cats: A physiological study. Journal of Comparative Neurology 171, 229–245.Google Scholar
Shatz, C.J. (1977c). Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats. Journal of Comparative Neurology 173, 497–518.CrossRefGoogle ScholarPubMed
Stone, J. (1966). The nasotemporal division of the cat's retina. Journal of Comparative Neurology 126, 585–599.Google ScholarPubMed
Stone, J., Rowe, M.H. & Campion, J.E. (1978). Retinal abnormalities in the Siamese cat. Journal of Comparative Neurology 180, 773–782.CrossRefGoogle ScholarPubMed
Timney, B., Elberger, A.J. & Vandewater, M.L. (1985). Binocular depth perception in the cat following early corpus callosum section. Experimental Brain Research 60, 19–26.CrossRefGoogle ScholarPubMed
Timney, B. & Lansdown, G. (1989). Binocular depth perception, visual acuity and visual fields in cats following neonatal section of the optic chiasm. Experimental Brain Research 74, 272–278.CrossRefGoogle ScholarPubMed
Toyama, K., Matsunami, K., Ohno, T. & Tokashiki, S. (1974). An intracellular study of neuronal organization in the visual cortex. Experimental Brain Research 21, 45–66.CrossRefGoogle ScholarPubMed
Tremblay, F., Ptito, M., Lepore, F., Miceli, D. & Guillemot, J.P. (1987). Distribution of visual callosal projection neurons in the Siamese cat: An HRP study. Journalfür Hirnforschung 285, 491–503.Google Scholar
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.CrossRefGoogle ScholarPubMed
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. Journal of Comparative Neurology 185, 657–678.CrossRefGoogle Scholar
Voigt, T., Levay, S. & Stevens, M.A. (1988). Morphological and immunocytochemical observations on the visual callosal projections in the cat. Journal of Comparative Neurology 272, 450–460.CrossRefGoogle ScholarPubMed
Westheimer, G. & Mitchell, D.E. (1969). The sensory stimulus for disjunctive eye movements. Vision Research 9, 749–755.CrossRefGoogle ScholarPubMed
Whitteridge, D. & Clarke, P.G.H. (1982). Ipsilateral visual field represented in the cat's visual cortex. Neuroscience 7, 1855–1860.CrossRefGoogle ScholarPubMed
Wiitanen, J.T. (1969). Selective silver impregnation of degenerating axons and axon terminals in the central nervous system of the monkey (Macaca mulatto). Brain Research 14, 546–548.CrossRefGoogle Scholar
Wilkes, M., Grant, S. & Berman, N. (1986a). Callosal connections between areas 17 and 18 of normal and Siamese cat cortexd: A quantitative study. Investigative Ophthalmology and Visual Science (Suppl.) 25, 233.Google Scholar
Wilkes, M., Grant, S. & Berman, N. (1986b). Abnormal callosal connections in Siamese cats are independent of strabismus. Society for Neuroscience Abstracts 12, 1370.Google Scholar
Wilson, M.E. (1968). Cortico-cortical connections of the cat visual areas. Journal of Anatomy 102, 375–386.Google ScholarPubMed
Wise, S.P. & Jones, E.G. (1976). The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. Journal of Comparative Neurology 168, 313–344.CrossRefGoogle ScholarPubMed
Yinon, U., Chen, M., Zamir, S. & Gelerstein, S. (1988). Corpus callosum transection reduces binocularity of cells in the visual cortex of adult cats. Neuroscience Letters 92, 280–284.CrossRefGoogle ScholarPubMed