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Transcallosal circuitry revealed by blocking and disinhibiting callosal input in the cat

Published online by Cambridge University Press:  02 June 2009

Jun-Shi Sun ,
B. Li ,
M. H. Ma  and
Y. C. Diao
Jun-Shi Sun
Affiliation:
Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston Department of Visual Information Processing, Institute of Biophysics, Academia Sinica, Beijing, 100101, The People’s Republic of China
B. Li
Affiliation:
Department of Visual Information Processing, Institute of Biophysics, Academia Sinica, Beijing, 100101, The People’s Republic of China
M. H. Ma
Affiliation:
Department of Visual Information Processing, Institute of Biophysics, Academia Sinica, Beijing, 100101, The People’s Republic of China
Y. C. Diao
Affiliation:
Department of Visual Information Processing, Institute of Biophysics, Academia Sinica, Beijing, 100101, The People’s Republic of China
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Abstract

The purpose of this study was to obtain quantitative measures of the influence of callosal input to cells at the area 17/18 border region where transcallosal axons terminate most densely. Single-cell recordings were performed at the area 17/18 border region of the right hemisphere, while gamma-aminobutyric acid (GABA) or its antagonist, bicuculline, were applied to the transcallosal projecting regions of the left hemisphere to either block or overactivate the cells which projected to the neurons at the recording site. The results showed that visually evoked responses of the cells at the area 17/18 border were affected by administration of GABA or bicuculline to the contralateral hemisphere. Blockade of transcallosal input by application of GABA in the left hemisphere diminished the visually evoked responses of 51% of the neurons in the right hemisphere, and led to an increase in response magnitude for 17% of the neurons. Disinhibition of transcallosal input by application of bicuculline increased the evoked activity of 40% of the neurons and diminished the response magnitude of 20% of the neurons in the right hemisphere. GABA and bicuculline failed to show antagonistic effects on some cells. Thirty-two percent of the cells were affected by only one type of drug administration, and 13% of the cells showed either an increase or a decrease in responses after both GABA and then bicuculline administration. This study demonstrated complex interactions between neurons connected by the transcallosal pathway. A model of the transcallosal circuitry was proposed to explain the results.

Keywords

Corpus callosumVisual cortexArea 17/18 borderGABABicucullineCat
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 2 , March 1994 , pp. 189 - 197
Copyright
Copyright © Cambridge University Press 1994

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References

Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth discrimination. Journal of Physiology 193, 327–342.CrossRefGoogle ScholarPubMed
Berlucchi, G. (1972). Anatomical and physiological aspects of visual functions of corpus callosum. Brain Research 37, 371–392.CrossRefGoogle ScholarPubMed
Berlucchi, G. & Rizzolatti, G. (1968). Binocularly driven neurons in visual cortex of split-chiasm cats. Science 159, 308–310.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 naso-temporal division. Journal of Physiology 205, 471–497.CrossRefGoogle Scholar
Blakemore, C. (1970). Binocular depth perception and the optic chiasm. Vision Research 10, 43–47.CrossRefGoogle ScholarPubMed
Blakemore, C., Diao, Y., Pu, M., Wang, Y. & Xiao, Y. (1983). Possible functions of the interhemispheric connexions between visual cortical areas in the cat. Journal of Physiology 337, 331–349.CrossRefGoogle ScholarPubMed
Bloz, J. & Gilbert, C.D. (1986). Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320, 362–365.CrossRefGoogle Scholar
Buhl, E.H. & Singer, W. (1989). The callosal projection in cat visual cortex as revealed by a combination of retrograde tracing and intracellular injection. Experimental Brain Research 75, 470–476.CrossRefGoogle ScholarPubMed
Chang, W.-B., Fang, X. & Diao, Y.-C. (1988). Effects of elimination of callosal transmission by cortical cooling on some characteristics of cortical cells in the 17/18 border region of cats. Acta Biophysica Sinica 4, 309–315 (in Chinese).Google 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
Cynader, M.C., Gardner, J.C., Lepore, F. & Guillemot, J.P. (1986). Interhemispheric communication and binocular vision: Functional and developmental aspects. In Two Hemispheres-One Brain: Functions of the Corpus Callosum, ed. Lepore, F., Ptito, M. & Jasper, H.H., pp. 189–209. New York: Alan R. Liss.Google Scholar
Diao, Y.C., Jla, 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
Eldridge, J. (1979). Reversible ophthalmoscope using a corner-tube. Journal of Physiology 295, 1–2P.Google Scholar
Fisken, R.A., Garey, L.J. & Powell, T.P.S. (1975). The intrinsic association and commissural connections of area 17 of the visual cortex. Philosophical Transactions of the Royal Society B (London) 272, 487–536.Google ScholarPubMed
Gabbott, P.L.A., Martin, K.A.C. & Whitteridge, D. (1987). Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17). Journal of Comparative Neurology 259, 364–381.CrossRefGoogle ScholarPubMed
Gilbert, C.D. (1983). Microcircuitry of the visual cortex. Annual Review of Neuroscience 6, 217–247.CrossRefGoogle ScholarPubMed
Gray, E.G. (1959). Axosomatic and axodendritic synapses of the cerebral cortex: An electron microscope study. Journal of Anatomy 93, 420–434.Google ScholarPubMed
Harvey, A.R. (1980). A physiological analysis of subcortical and commissural projections of areas 17 and 18 of the cat. Journal of Physiology 302, 507–534.CrossRefGoogle ScholarPubMed
Houser, C.R., Vaughn, J.E., Hendry, S.H.C., Jones, E.G. & Peters, A. (1984). GABA neurons in the cerebral cortex. In Cerebral Cortex, Vol. 2, Functional Properties of Cortical Cells, ed. Jones, E.G. & Peters, A., pp. 63–89. New York: Plenum Press.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1967). Cortical and callosal connections concerned with the vertical meridian of visual fields in the cat. Journal of Neurophysiology 30, 1561–1573.CrossRefGoogle ScholarPubMed
Innocenti, G.M. (1980). The primary visual pathway through the corpus callosum: Morphological and functional aspects in the cat. Archives Italienne Biologie 118, 124–188.Google ScholarPubMed
Levay, S. (1973). Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. Journal of Comparative Neurology 150, 53–86.CrossRefGoogle Scholar
Martin, K.A.C., Somogyi, P. & Whitteridge, D. (1983). Physiological and morphological properties of identified basket cells in the cat’s visual cortex. Experimental Brain Research 50, 193–200.Google ScholarPubMed
McCourt, M.E., Thalluri, J. & Henry, G.H. (1990). Properties of area 17/18 border neurons contributing to the visual transcallosal pathway in the cat. Visual Neuroscience 5, 83–98.CrossRefGoogle Scholar
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical & Biological Engineering 10, 662–672.CrossRefGoogle ScholarPubMed
Payne, B.R. (1986). Role of callosal cells in the functional organization of cat striate cortex. In Two Hemispheres-One Brain: Functions of the Corpus Callosum, ed. Lepore, F., Ptito, M. & Jasper, H.H., pp. 231–254. New York: Alan R. Liss.Google Scholar
Payne, B.R. (1991). The visual-field map in the transcallosal sending zone of area 17 in the cat. Visual Neuroscience 7, 201–219.CrossRefGoogle ScholarPubMed
Payne, B.R. & Siwek, D.F. (1991). Visual-field map in the callosal recipient zone at the border between areas 17 and 18 in the cat. Visual Neuroscience 7, 221–236.CrossRefGoogle ScholarPubMed
Payne, B.R., Siwek, D.F. & Lomber, S.G. (1991). Complex transcallosal interactions in visual cortex. Visual Neuroscience 6, 283–289.CrossRefGoogle ScholarPubMed
Peters, A. & Fairen, A. (1978). Smooth and sparsely-spined stellate cells in the visual cortex of the rat: A study using a combined Golgielectron microscope technique. Journal of Comparative Neurology 181, 129–172.CrossRefGoogle Scholar
Peters, A., Payne, B.R. & Josephson, K. (1990). Transcallosal non-pyramidal cell projections from visual cortex in the cat. Journal of Comparative Neurology 302, 124–142.CrossRefGoogle ScholarPubMed
Peters, A., Proskauer, C.C. & Ribak, C.E. (1982). Chandelier cells in rat visual cortex. Journal of Comparative Neurology 206, 397–416.CrossRefGoogle ScholarPubMed
Peters, A. & Regidor, J. (1981). A reassessment of the forms of non-pyramidal neurons in area 17 of cat visual cortex. Journal of Comparative Neurology 203, 685–716.CrossRefGoogle Scholar
Podell, M., Yinon, U. & Hammer, A. (1984). Properties of visual cortical cells of the intact and the deafferented hemisphere of unilateral optic tract sectioned acute and chronic adult cats. Experimental Brain Research 55, 91–96.CrossRefGoogle ScholarPubMed
saint-Marie, R.L. & Peters, A. (1985). The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): A Golgi-electron microscopic study. Journal of Comparative Neurology 233, 213–235.CrossRefGoogle 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 (1982). The distribution of the cells of origin of callosal projections in cat visual cortex. Journal of Neuroscience 2, 1079–1089.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1977). Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats. Journal of Comparative Neurology 173, 497–518.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1975). The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat’s striate cortex. Journal of Physiology 250, 287–304.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1977 a). Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat’s visual cortex. Journal of Physiology 271, 699–720.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1977 b). The contribution of excitatory and inhibitory inputs to the length preference of hypercomplex cells in layers II and III of the cat’s striate cortex. Journal of Physiology 273, 775–790.CrossRefGoogle Scholar
Sillito, A.M. (1979). Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. Journal of Physiology 289, 33–53.CrossRefGoogle ScholarPubMed
Somogyi, P. (1977). A specific ‘axo-axonal’ interneuron in the visual cortex of the rat. Brain Research 136, 345–350.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
Vesbaeya, C., Whitteridge, D. & Wilson, M.E. (1967). Callosal connexions of the cortex representing the area centralis. Journal of Physiology 191, 79–80P.Google Scholar
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