Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-28T17:40:21.964Z Has data issue: false hasContentIssue false
  • English
  • Français

Organization of reciprocal connections between area 17 and the lateral suprasylvian area of cat visual cortex

Published online by Cambridge University Press:  02 June 2009

Stewart Shipp  and
Simon Grant
Stewart Shipp
Affiliation:
Department of Anatomy and Developmental Biology, University College, London, UK Department of Anatomy, The Medical College of Pennsylvania, Philadelphia
Simon Grant
Affiliation:
Department of Anatomy and Developmental Biology, University College, London, UK Department of Anatomy, The Medical College of Pennsylvania, Philadelphia
Get access Rights & Permissions [Opens in a new window]

Abstract

The lateral suprasylvian (LS) area (or Clare-Bishop area) is a region of visual cortex in the cat which has been defined as an isolated projection zone of area 17 (VI or striate cortex) within the suprasylvian sulcus. We have studied the overall topography and detailed pattern of connection between these two visual areas following injections of WGA-HRP into one or the other.

The projection from area 17 to LS is formed largely (-90%) from supragranular layer neurons that are distributed, in the coronal plane, in multiple regularly spaced patches. These patches are especially prominent in regions of area 17 representing central vision along and around the horizontal meridian. In reconstructions of serial coronal sections, and in flatmounts of the same region, the patches are seen to align so that in the plane tangential to the cortical surface they appear as a system of parallel bands whose main axis of elongation is rostro-ventral to caudo-dorsal, or near parallel to the area 17/18 border. The mean periodicity of the bands is about 1.0 mm.

The projection from area 17 terminates mainly in layers 4, 3, and 2 of area LS, and also appears patchy in the coronal plane. Reconstruction of the cortical surface view again reveals a system of rostrocaudal bands, but with a mean periodicity of 2 mm. The back projection is less periodically organized, arising predominantly (-80%) from a continuous sheet of infragranular neurons in area LS and terminating mainly in layer 1 of area 17, across the underlying patch and interpatch zones of the supragranular projection cells. However, neurons in layers 2 and upper 3 of area LS, which form the minority origin of the back projection, are mostly located in columnar registration with the patches of area 17 terminals.

The bands of supragranular layer neurons projecting to area LS are aligned obliquely to the iso-orientation domains of area 17, indicating a further component to its organization. It is suggested that this may correspond to a segregation of the X and Y channels in area 17, with outputs to area LS selectively arising from the Y pathway, in accordance with previous reports.

Keywords

Projection bandsTermination bandsX pathwaysY pathways
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 4 , April 1991 , pp. 339 - 355
Copyright
Copyright © Cambridge University Press 1991

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., (1979). 14-C-deoxyglucose mapping of orientation subunits in the cat's visual cortical areas. Specificity of intrinsic in primate primary visual cortex. Journal of Neuroscience 4, 2830–2835.Google Scholar
Lowel, S., Freeman, B., & Singer, W., (1987). Topographic organization of the orientation column system in large flat-mounts of the cat visual cortex: a 2-deoxyglucose study. Journal of Comparative Neurology 255, 401–415.CrossRefGoogle ScholarPubMed
Lowel, S., Bischof, H.-J., Leutenecker, B.Singer, W. (1988). Topographic relations between ocular dominance and orientation columns in the cat striate cortex. Experimental Brain Research 71, 33–46.CrossRefGoogle ScholarPubMed
Lund, J.S., Henry, G.H., Macqueen, C.L. & Harvey, A.R. (1979). Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the monkey. Journal of Comparative Neurology 184, 599–618.CrossRefGoogle Scholar
Maclewicz, R.J. (1974). Afferents to the lateral suprasylvian gyrus of the cat traced with horseradish peroxidase. Brain Research 78, 139–143.CrossRefGoogle Scholar
Martin, K.A.C., & Whitteridge, D., (1984). Form, function, and intracortical projections of spiny neurons in the striate cortex of the cat. Journal of Physiology (London) 353, 463–504.CrossRefGoogle ScholarPubMed
Maske, R., Yamane, S. & Bishop, P.O., (1985). Simple and B-cells in cat striate cortex. Complementarity of responses to moving light and dark bars. Journal of Neurophysiology 53, 670–685.CrossRefGoogle ScholarPubMed
Mesulam, M.M., (1982). Tracing Neural Connections with Horseradish Peroxidase. New York: Wiley.Google Scholar
Mitchison, G., & Crick, F.H.C., (1982). Long axons within the striate cortex: their distribution, orientation, and patterns of connection. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3661–3665.CrossRefGoogle ScholarPubMed
Mithison, G.J., (1985). Does the striate cortex contain a system of oriented axons? In Models of the Visual Cortex, ed.Rose, D. & Dobson, V.G., pp. 443–451. Chichester: John Wiley.Google Scholar
Mitzdore, U., & Singer, W. (1978). Prominent excitatory pathways in the cat visual cortex (A17 and A18): a current source density analysis of electrically evoked potentials. Experimental Brain Research 33, 371–394.Google Scholar
Montero, V.M. (1981). Topography of the cortico-cortical connections from the striate cortex in the cat. Brain, Behaviour, and Evolution 18, 194–218.Google ScholarPubMed
Morrone, M.C., Distefano, M. & Burr, D.C. (1986). Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat. Journal of Neurophysiology 56, 969–986.CrossRefGoogle ScholarPubMed
Movshon, J.A., Thompson, I.D., & Tolhurst, D.J., (1978). Spatial Summation in the receptive fields of simple cells in the cat's striate cortex. Journa of physiology (London) 283, 53–77.CrossRefGoogle ScholarPubMed
Mullikin, W.H., Jones, J.P., & Palmer, L.A., (1984). Receptive-field properties and laminar distribution of X-like and Y-like simple cells in cat area 17. Journal of Neurophysiology 52, 350–371.CrossRefGoogle ScholarPubMed
Orban, G.A.,Kennedy, H. & Maes, H.M (1981a). Response to movement of neurons in areas 17 and 18 of the cat: velocity sensitivity. Journal of Neurophysiology 45, 1043–1058.CrossRefGoogle ScholarPubMed
Orban, G.A., Kennedy, H., & Maes, H., (1981b) Response movement of neurons in areas 17 and 18 of the cat: direction selectivity. Journal of Neurophysiology 45, 1059–1073.CrossRefGoogle ScholarPubMed
Otsuka, R., & Hassler, R., (1962). Uber aufbau und gliederung der corticalen sehsphare bei der katze. Archiv fur Psychiatrie und Zeitschrift f.d. ges. Neurologie 203, 212–234.CrossRefGoogle Scholar
Price, D.J., & Blakemore, C. (1985). The postnatal development of the association projection from visual cortical area 17 to area 18 in the cat. Journal of Neuroscience 5, 2443–2452.CrossRefGoogle ScholarPubMed
Price, D.J., & Zumbroich, T.J. (1989). Postnatal development of corticocortical efferents from area 17 in the cat's visual cortex. Journal of Neuroscience 9, 600–613.CrossRefGoogle ScholarPubMed
Raczkowski, D., & Rosenquist, A.C., (1983). Connections of the multiple visual cortical areas with the lateral posterior-pulvinar complex and adjacent thalamic nuclei in the cat. Journal of Neuroscience 3, 1912–1942.CrossRefGoogle ScholarPubMed
Rauschecker, J.P., Von Grunau, M.W., & Poulin, C. (1987 a). Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing. Journal of Neuroscience 7, 943–958.CrossRefGoogle ScholarPubMed
Rauschecker, J.P., Von Grunau, M.W., & Poulin, C., (1987b) Thalamo-cortical connections and their correlation with receptive field properties in the cat's lateral suprasylvian visual cortex. Experimental Brain Research 67, 100–112.CrossRefGoogle ScholarPubMed
Rockland, K.S., &Lund, J.S., (1983). lntrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 303–318.CrossRefGoogle Scholar
Salin, P.A., Bullier, J. &Kennedy, H., (1989). Convergence and divergence in the afferent projections to cat area 17. Journal of Comparative Neurology 283, 486–512.CrossRefGoogle ScholarPubMed
Sanides, F., &Hoffmann, J. (1969). Cyto- and myelo-architecture of the visual cortex of the cat and of the surrounding integration cortices. Journal fur Hirnforschung 11, 79–104.Google Scholar
Segraves, M.A., &Rosenquist, A.C. (1982). The afferent and efferent callosal connections of retinotopically defined areas in cat cortex. Journal of Neuroscience 2, 1090–1107.CrossRefGoogle ScholarPubMed
Shatz, C.J., Lindstrom, S., &Wiesel, T.N. (1977). The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Research 131, 103–116.CrossRefGoogle ScholarPubMed
Sherk, H. (1986a). Location and connections of visual cortical areas in the cat's suprasylvian sulcus. Journal of Comparative Neurology 247, 1–31.CrossRefGoogle ScholarPubMed
Sherk, H. (1986 b). Coincidence of patchy inputs from the lateral nucleus and area 17 to the cat's Clare-Bishop area. Journal of Comparative Neurology 253, 105–120.CrossRefGoogle Scholar
Sherk, H., &Ombrellaro, M., (1988). The retinotopic match between area 17 and its targets in visual suprasylvian cortex. Experimental Brain Research 72, 225–236.CrossRefGoogle ScholarPubMed
Sherk, H. (1989). Visual response properties of cortical inputs to an extrastriate area in the cat. Visual Neuroscience 3, 249–265.CrossRefGoogle Scholar
Shipp, S., &Zeki, S., (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–325.CrossRefGoogle ScholarPubMed
Shipp, S., &Zeki, S. (1989a). The organization of connections between areas V5 and Vl in macaque monkey visual cortex. European Journal of Neuroscience 1, 309–332.CrossRefGoogle Scholar
Shipp, S. &Zeki, S., (1989b). The organization of connections between areas V5 and V2 in macaque monkey visual cortex. European Journal of Neuroscience 1, 333–354.CrossRefGoogle ScholarPubMed
Singer, W. (1981). Topographic organization of orientation columns in the cat visual cortex. Experimental Brain Research 44, 431–436.CrossRefGoogle ScholarPubMed
Spear, P.D., &Baumann, T.P. (1975). Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 38, 1403–1420.CrossRefGoogle ScholarPubMed
Spera, P.D., &Baumann, T.P. (1979). Effects of visual cortex removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 42, 31–56.CrossRefGoogle Scholar
Stone, J., (1978). The number and distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 180, 753–772.CrossRefGoogle ScholarPubMed
Stone, J., &Dreher, B., (1973). Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. Journal of Neurophysiology 36, 551–567.CrossRefGoogle ScholarPubMed
Sugiyama, M., (1979). The projection of the visual cortex on the ClareBishop area in the cat: a degeneration study with the electron microscope. Experimental Brain Research 36, 433–443.CrossRefGoogle Scholar
Swindale, N.V., Matsubara, J.A., &Cynader, M.S. (1987). Surface organization of orientation and direction selectivity in cat area 18. Journal of Neuroscience 7, 1414–1427.CrossRefGoogle ScholarPubMed
Symonds, L.L. &Rosenquist, A.C. (1984). Cortico-cortical connections among the visual areas in the cat. Journal of Comparative Neurology 229, 1–38.CrossRefGoogle Scholar
Tanaka, K., (1983a). Distinct X- and Y-streams in the cat visual cortex revealed by bicuculline application. Brain Research 265, 143–147.CrossRefGoogle ScholarPubMed
Tanaka, K., (1983 b). Cross-correlation of geniculostriate neuronal relationships in cats. Journal of Neurophysiology 49, 1303–1318.CrossRefGoogle ScholarPubMed
Tieman, S.B. &Tumos, N. (1983). [14C] -2-Deoxyglucose demonstration of the organization of ocular dominance in areas 17 and 18 the normal cat. Brain Research 267, 35–46.CrossRefGoogle ScholarPubMed
Tong, L.,Kalil, R.E. &Spear, P.D., (1982). Thalamic projections to visual areas of the middle suprasylvian sulcus of the cat. Journal of Comparative Neurology 212, 103–117.CrossRefGoogle ScholarPubMed
Tong, L., &Spear, P.D. (1986). Single thalamic neurons project to both lateral suprasylvian visual cortex and area 17: a retrograde fluorescent double-labeffing study. Journal of Comparative Neurology 246, 254–264.CrossRefGoogle ScholarPubMed
Tooteli, R.B.,Silverman, M.S., &De Valois, R.L. (1981). Spatial frequency columns in primary visual cortex. Science 214, 813–815.CrossRefGoogle Scholar
Tretter, F., Cynader, M., & Singer, W. (1975). Cat parastriate cortex: a primary or secondary area? Journal of Neurophysiology 38, 1099–1113.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A., & Rosenqusit, A.C., (1978). The retinotopic organization of area 17(striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.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, 11–28.CrossRefGoogle ScholarPubMed
Zeki, S. & Smipp, S. (1988). The functional logic of cortical connections. Nature 335, 311–317.CrossRefGoogle ScholarPubMed
Zeki, S. & Shipp, S. (1989). Modular connections between areas V2 and V4 of the macaque monkey visual cortex. European Journal of Neuroscience 1, 494–506.CrossRefGoogle ScholarPubMed
Zumbroich, T.J. & Blakemore, C. (1987). Spatial and temporal selectivity in the suprasylvian visual cortex of the cat. Journal of Neuroscience 7, 482–500.CrossRefGoogle ScholarPubMed