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Visuotopic organization of the lateral suprasylvian area and of an adjacent area of the ectosylvian gyrus of cat cortex: A physioligical and connectional study

Published online by Cambridge University Press:  02 June 2009

Simon Grant  and
Stewart Shipp
Simon Grant
Affiliation:
Department of Anatomy and Developmental Biology, University College London, Gower Street, London WCIE 6BT, England, U.K
Stewart Shipp
Affiliation:
Department of Anatomy and Developmental Biology, University College London, Gower Street, London WCIE 6BT, England, U.K
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Abstract

We have explored the visuotopic organization of the territory surrounding the middle suprasylvian sulcus (MSS) of cat cerebral cortex by electrophysiological mapping, and by tracing the topography of its cortical and subcortical connections using wheatgerm-agglutinin horseradish peroxidase (WGA-HRP). Observations from the two approaches were concordant, and confirmed the presence of two separate visual areas in the MSS that approximate, but do not exactly correspond, to the location and internal organization of the posterior medial and posterior lateral lateral suprasylvian (PMLS, PLLS) areas of Palmer et al. (1978).

We define as part of the lateral suprasylvian (LS) area the territory on the medial bank and caudal end of the lateral bank of the MSS that receives a topographically organized projection from the region of area 17 representing the lower visual quadrant. This territory is connected with other structures that are themselves striate-recipient (cortical areas 18 and 19, and the lateral division of the lateral posterior (LPI) nucleus), and with a variety of nuclei that receive direct retinal input, such as the C-laminae of the LGd, the medial interlaminar nucleus (MIN), and the superficial layers of the superior colliculus (SC). Its connections with the LP1, LGd, MIN, and SC correspond topographically with the input from area 17. Revised maps of area LS were produced from the physiological and connectional data: its rostral border is formed by a representation of lower visual elevations with the horizontal meridian represented caudally, and its lateral border is formed by the vertical meridian; area LS shares a representation of the center of gaze with the visual area of the lateral bank at its caudal end.

The adjacent lateral bank area has larger receptive fields than area LS, and very different connectivity. It receives no input from area 17 and little input from striate-recipient structures, including area LS, but instead is connected to more remote extrastriate visual areas, such as the anterior ectosylvian visual (AEV) area in insular cortex, and to zones of the thalamus in receipt of tectal input (LPm and the lateromedial-suprageniculate nuclear complex). According to both mapping approaches, the lateral bank area contains representations of both the upper and lower visual quadrants but a rather limited degree of visuotopic order. We refer to it as the posterior ectosylvian visual (PEV) area, because it appears to be functionally and connectionally dissociated from area LS, but is possibly a functional antecedent of area AEV.

Keywords

Extrastriate visual cortexArea 17 projectionRetinotopic mappingTectal map
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 4 , April 1991 , pp. 315 - 338
Copyright
Copyright © Cambridge University Press 1991

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References

Albus, K., & Beckmann, R. (1980) Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location. Journal of Physiology (London) 299, 247–276.CrossRefGoogle ScholarPubMed
Allman, J.M., & Kaas, J.H. (1975). The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus Irivirgatus). Brain Research 100, 473–487.CrossRefGoogle Scholar
Bowman, E.M. & Olson, C.R. (1988 a). Visual and auditory association areas of the cat's posterior ectosylvian gyrus: thalamic afferents. Journal of Comparative Neurology 272, 15–29.CrossRefGoogle ScholarPubMed
Bowman, E.M. & Olson, C.R. (1988 b). Visual and auditory association areas of the cat's posterior ectosylvian gyrus: cortical afferents. Journal of Comparative Neurology 272, 30–42.CrossRefGoogle ScholarPubMed
Clare, M.H. & Bishop, G.H. (1954). Responses from an association area secondarily activated from optic cortex. Journal of Neurophysiology 17, 271–277.CrossRefGoogle ScholarPubMed
Djavadian, R.L. & Harutiunian-Kozak, B.A. (1983). Retinotopic organization of the lateral suprasylvian area of the cat. Acta Neurobiologiae Experimentalis 43, 251–262.Google ScholarPubMed
Dubner, R. & Rutledge, L.T. (1964). Recording and analysis of converging input upon neurons in cat association cortex. Journal of Neurophysiology 27, 620–634.CrossRefGoogle ScholarPubMed
Dubner, R. & Rutledge, L.T. (1965). Intracellular recording of the convergence of input upon neurons in cat association cortex. Experimental Neurology 12, 349–369.CrossRefGoogle ScholarPubMed
Dubner, R. & Brown, F.J. (1968). Response of cells to restricted visual stimuli in an association area of cat cerebral cortex. Experimental Neurology 20, 70–86.CrossRefGoogle Scholar
Feldon, S., Feldon, P. & Kruger, L. (1970). Topography of the retinal projection upon the superior colliculus in the cat. Vision Research 10, 135–143.CrossRefGoogle ScholarPubMed
Forssberg, H. & Svartengren, G. (1983). Hard-wired locomotor network in cat revealed by a retained motor pattern to gastrocnemius after muscle transposition. Neuroscience Letters 41, 283–288.CrossRefGoogle Scholar
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, Neurosurgery, and Psychiatry 31, 135–157.Google ScholarPubMed
Gibson, J.J. (1950). The Perception of the Visual World. Boston: Houghton Mifflin.Google Scholar
Graybiel, A.M. & Berson, D.M. (1980). Histochemical identification and afferent connections of subdivisions in the lateralis posterior-pulvinar complex and related thalamic nuclei in the cat. Neuroscience 5, 1175–1238.CrossRefGoogle ScholarPubMed
Guillery, R.W., Geisert, E.E., Polley, E.H. & Mason, C.A. (1980). Analysis of the retinal afferents to the cat's medial interlaminar nucleus and to its rostral thalamic extension, the “geniculate wing.” Journal of Comparative Neurology 194, 117–142.CrossRefGoogle Scholar
Hammond, P. (1978). Inadequacy of nitrous oxide/oxygen mixtures for maintaining anaesthesia in cats: satisfactory alternatives. Pain 5, 143–151.CrossRefGoogle ScholarPubMed
Heath, C.J. & Jones, E.G. (1971). The anatomical organization of the suprasylvian gyrus of the cat. Ergebnisse der Anatomie und Entwicklungsgeschichte 45, 1–64.Google ScholarPubMed
Hicks, T.P., Watanabe, S., Miyake, A. & Shoumura, K. (1984). Organization and properties of visually responsive neurons in the suprageniculate nucleus of the cat. Experimental Brain Research 55, 359–367.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1969). Visual area of the lateral suprasylvian gyrus (Clare-Bishop area) of the cat. Journal of Physiology (London) 202, 251–260.CrossRefGoogle ScholarPubMed
Hutchins, B. & Updyke, B.V. (1989). Retinotopic organization within the lateral posterior complex of the cat. Journal of Comparative Neurology 285, 350–398.CrossRefGoogle ScholarPubMed
Kaneseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319–337.CrossRefGoogle Scholar
Kaufman, E.F.S. & Rosenquist, A.C. (1985). Efferent projections of the thalamic intralaminar nuclei in the cat. Brain Research 335, 257–279.CrossRefGoogle ScholarPubMed
Komatsu, Y., Shibuki, K. & Toyama, K. (1983). Eye movement-related activities in cells of the lateral suprasylvian cortex of the cat. Neuroscience Letters 41, 271–276.CrossRefGoogle ScholarPubMed
Lashley, K.S. & Clark, G. (1946). The cytoarchitecture of cerebral cortex of Ateles: a critical examination of architectonic studies. Journal of Comparative Neurology 85, 223–305.CrossRefGoogle ScholarPubMed
Marshall, W.H., Talbot, S.A. & Ades, H.W. (1943). Cortical responses of the anesthetized cat to gross photic and electrical afferent stimulation. Journal of Neurophysiology 6, 1–15.CrossRefGoogle Scholar
Mason, R. (1978). Functional organization of the cat's pulvinar complex. Experimental Brain Research 31, 51–66.CrossRefGoogle ScholarPubMed
Merrill, E.G. & Atnsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical, Electrical, and Biological Engineering 10, 662–672.CrossRefGoogle ScholarPubMed
Mesulam, M. M. (1982). Tracing Neural Connections with Horseradish Peroxidase. New York: Wiley.Google Scholar
Montero, V.M. (1981). Topography of the cortico-cortical connections from the striate cortex in the cat. Brain, Behavior, and Evolution 18, 194–218.CrossRefGoogle ScholarPubMed
Mucke, L., Norita, M., Benedek, G. & Creutzfeldt, O. (1982). Physiologic and anatomic investigation of visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat. Experimental Brain Research 46, 1–11.CrossRefGoogle ScholarPubMed
Norita, M., Mucke, L., Benedek, G., Albowitz, B., Yatoh, K. & Creutzfeldt, O.D. (1986). Connections of the anterior ectosylvian visual area (AEV). Experimental Brain Research 62, 225–240.CrossRefGoogle ScholarPubMed
Olson, C.R. & Graybiel, A.M. (1987). Ectosylvian visual area of the cat: location, retinotopic organization, and connections. Journal of Comparative Neurology 261, 277–294.CrossRefGoogle ScholarPubMed
Olson, C.R. & Lawler, K. (1987). Cortical and subcortical afferent connections of a posterior division of feline area 7 (Area 7p). Journal of Comparative Neurology 259, 13–30.CrossRefGoogle ScholarPubMed
Otsuka, R. & Hassler, R. (1962). Uber aufbau und gliederung der corticalen sehsphare bei der katze. Archiv für Psychiatrie und Nervenkrankheiten 203, 212–234.CrossRefGoogle Scholar
Palmer, L.A., Rosenquist, A.C. & Tusa, R.J. (1978). The retinotopic organization of lateral suprasylvian visual areas in the cat. Journal of Comparative Neurology 177, 237–256.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Rosenquist, A.C. (1981). Retinotopic organization in the cat lateral posterior-pulvinar complex. Brain Research 221, 185–191.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
Rauscheker, J.P., Von Grunau, M.W. & Poulin, C. (1987). 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 Scholar
Robertson, R.T. (1977). Thalamic projections to parietal cortex. Brain Research 14, 161–184.Google ScholarPubMed
Robertson, R.T. & Cunningham, T.J. (1981). Organization of corticothalamic projections from parietal cortex in the cat. Journal of Comparative Neurology 199, 569–585.CrossRefGoogle Scholar
Rosenquist, A.C. (1985). Connections of visual areas in the cat. In Cerebral Cortex, Vol. 3: Visual Cortex, ed. Peters, A. & Jones, E.G., pp. 81–117. New York: Plenum Press.Google Scholar
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. Journal of Comparative Neurology 143, 101–118.CrossRefGoogle Scholar
Sandies, F. & Hoffmann, J. (1969). Cyto- and myelo-architecture of the visual cortex of the cat and of the surrounding integration cortices. Journal für Hirnforschung 11, 79–104.Google Scholar
Segal, R.L. & Beckstead, R.M. (1984). The lateral suprasylvian corticotectal projection in cats. Journal of Comparative Neurology 225, 259–275.CrossRefGoogle ScholarPubMed
Skerk, H. (1986). Location and connections of visual cortical areas in the cat's suprasylvian sulcus. Journal of Comparative Neurology 247, 1–31.Google 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
Shook, B.L., Abramson, B.P. & Chalupa, L.M. (1984). An analysis of the transport of WGA-HRP in the cat's visual system. Journal of Neuroscience Methods 11, 65–77.CrossRefGoogle ScholarPubMed
Shoumura, K. (1972). Patterns of fiber degeneration in the lateral wall of the suprasylvian gyrus (Clare-Bishop area) following lesions in the visual cortex in cats. Brain Research 43, 264–267.CrossRefGoogle ScholarPubMed
Shoumura, K. & Itoh, K. (1972). Intercortical projections from the lateral wall of the suprasylvian gyrus, the Clare-Bishop area, of the cat. Brain Research 39, 536–539.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
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
Symonds, L.L., Rosenquist, A.C., Edwards, S.B. & Palmer, L.A. (1981). Projections of the pulvinar-lateral posterior complex to visual cortical areas in the cat. Neuroscience 6, 1995–2020.CrossRefGoogle ScholarPubMed
Thompson, R.F., Johnson, R.H. & Hoopes, J.J. (1963 a). Organization of auditory, somatic sensory, and visual projection to association fields of cerebral cortex in the cat. Journal of Neurophysiology 26, 343–364.CrossRefGoogle ScholarPubMed
Thompson, R.F., Smith, H.E. & Bliss, D. (1963 b). Auditory, somatic sensory, and visual response interactions and interrelations in association and primary cortical fields of the cat. Journal of Neurophysiology 26, 365–378.CrossRefGoogle ScholarPubMed
Tong, L., Kalil, R.E. & Spear, P.D. (1982). Thalamic projections to visual areas of the middle suprasylvian sulcus in the cat. Journal of Comparative Neurology 212, 103–117.CrossRefGoogle ScholarPubMed
Toyama, K., Fujii, K. & Umetani, K. (1990). Functional differentiation between the anterior and posterior Clare-Bishop cortex of the cat. Experimental Brain Research 81, 221–233.CrossRefGoogle ScholarPubMed
Turlesjski, K. & Michalski, A. (1975). Clare-Bishop area in the cat: location and retinotopical projection. Acta Neurobiologiae Experimentalis 35, 179–188.Google Scholar
Tusa, R.J. & Palmer, L.A. (1980). Retinotopic organization of areas 20 and 21 in the cat. Journal of Comparative Neurology 193, 147–164.CrossRefGoogle ScholarPubMed
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., Palmer, L.A. & Rosenquist, A.C. (1979). Retinotopic organization of areas 18 and 19 in the cat. Journal of Comparative Neurology 185, 657–678.CrossRefGoogle Scholar
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1981). Multiple cortical visual areas. Visual-field topography in the cat. In Cortical Sensory Organization, Vol. 2: Multiple Visual Areas, ed. Woolsey, C.N., pp. 1–31. Clifton, New Jersey: Humana Press.Google Scholar
Ungerleider, L.G. & Demsimone, R. (1986). Projections to the superior temporal sulcus from the central and peripheral field representations of V1. Journal of Comparative Neurology 248, 147–163.CrossRefGoogle Scholar
Updyke, B.V. (1981). Projections from visual areas of the middle suprasylvian sulcus onto the lateral posterior complex and adjacent thalamic nuclei in cat. Journal of Comparative Neurology 201, 477–506.CrossRefGoogle ScholarPubMed
Updyke, B.V. (1982). An additional retinotopically organized visual area (PS) within the cat's posterior suprasylvian sulcus and gyrus. Society for Neuroscience Abstracts 8, 810.Google Scholar
Updyke, B.V. (1986). Retinotopic organization within the cat's posterior suprasylvian sulcus and gyrus. Journal of Comparative Neurology 216, 265–280.CrossRefGoogle Scholar
Van Essen, D.C. (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3: Visual Cortex, ed. Peters, A. & Jones, E.G., pp. 259–329. New York: Plenum Press.Google Scholar
Von Grunau, M. & Frost, B.J. (1983). Double-opponent-process mechanism underlying RF structure of directionally specific cells of cat lateral suprasylvian area. Experimental Brain Research 49, 84–92.CrossRefGoogle Scholar
Von Grunau, M., Zumbroich, T.J. & Poulin, C. (1987). Visual receptive-field properties in the posterior suprasylvian cortex of the cat: a comparison between the areas PMLS and PLLS. Vision Research 27, 343–356.CrossRefGoogle Scholar
Woolsey, C.N. (1961). Organization of cortical auditory system. In Sensory Communication Systems, ed. Rosenblith, W.M., pp. 235–257. Cambridge: MIT Press.Google Scholar
Wright, M.J. (1969). Visual receptive fields of cells in a cortical area remote from the striate cortex in the cat. Nature 223, 973–975.CrossRefGoogle Scholar
Zeki, S.M. (1978). Functional specialization in the visual cortex of the rhesus monkey. Nature 274, 423–428.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
Zumbroich, T.J., Von Grunau, M., Poulin, C. & Blackmore, C. (1986). Differences of visual-field representation in the medial and lateral banks of the suprasylvian cortex (PMLS/PLLS) of the cat. Experimental Brain Research 64, 77–93.CrossRefGoogle ScholarPubMed