Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-08T00:36:39.578Z Has data issue: false hasContentIssue false

Retinotopic organization of ferret suprasylvian cortex

Published online by Cambridge University Press:  09 March 2006

GINA CANTONE
Affiliation:
Department of Biology, City College of the City University of New York, New York, New York Graduate Center of the City University of New York, New York, New York
JUN XIAO
Affiliation:
Department of Biology, City College of the City University of New York, New York, New York
JONATHAN B. LEVITT
Affiliation:
Department of Biology, City College of the City University of New York, New York, New York Graduate Center of the City University of New York, New York, New York

Abstract

The retinotopic organization of striate and several extrastriate areas of ferret cortex has been established. Here we describe the representation of the visual field on the Suprasylvian visual area (Ssy). This cortical region runs mediolaterally along the posterior bank of the suprasylvian sulcus, and is distinct from adjoining areas in anatomical architecture. The Ssy lies immediately rostral to visual area 21, medial to lateral temporal areas, and lateral to posterior parietal areas. In electrophysiological experiments we made extracellular recordings in adult ferrets. We find that single and multiunit receptive fields range in size from 2 deg × 4 deg to 21 deg × 52 deg. The total visual field representation in Ssy spans over 70 deg in azimuth in the contralateral hemifield (with a small incursion into the ipsilateral hemifield), and from +36 deg to −30 deg in elevation. There are often two representations of the horizontal meridian. Furthermore, the location of the transition from upper to lower fields varies among animals. General features of topography are confirmed in anatomical experiments in which we made tracer injections into different locations in Ssy, and determined the location of retrograde label in area 17. Both isoelevation and isoazimuth lines can span substantial rostrocaudal and mediolateral distances in cortex, sometimes forming closed contours. This topography results in cortical magnifications averaging 0.07 mm/deg in elevation and 0.06 mm/deg in azimuth; however, some contours can run in such a way that it is possible to move a large distance on cortex without moving in the visual field. Because of these irregularities, Ssy contains a coarse representation of the contralateral visual field.

Type
Research Article
Copyright
2006 Cambridge University Press

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

REFERENCES

Albright, T.D. & Desimone, R. (1987). Local precision of visuotopic organization in the middle temporal area (MT) of the macaque. Experimental Brain Research 65, 582592.Google Scholar
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, 159179.Google Scholar
Allman, J.M. & Kaas, J.H. (1971). Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Research 35, 89106.Google Scholar
Allman, J.M. & Kaas, J.H. (1974). The organization of the second visual area (V II) in the owl monkey: A second-order transformation of the visual hemifield. Brain Research 76, 247265.Google Scholar
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 trivirgatus). Brain Research 100, 473487.Google Scholar
Angelucci, A. & Bullier, J. (2003). Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? Journal of Physiology (Paris) 97, 141154.Google Scholar
Angelucci, A., Clasca, F., & Sur, M. (1996). Anterograde axonal tracing with the subunit B of cholera toxin: A highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains. Neuroscience Methods 65, 101112.Google Scholar
Angelucci, A., Levitt, J.B., Walton, E.J., Hupé, J.M., Bullier, J., & Lund, J.S. (2002). Circuits for local and global signal integration in primary visual cortex. Journal of Neuroscience 22, 86338646.Google Scholar
Baker, J.F., Petersen, S.E., Newsome, W.T., & Allman, J.M. (1981). Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): A quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. Journal of Neurophysiology 45, 397416.Google Scholar
Baker, G.E., Thompson, I.D., Krug, K., Smyth, D., & Tolhurst, D.J. (1998). Spatial-frequency tuning and geniculocortical projections in the visual cortex (areas 17 and 18) of the pigmented ferret. European Journal of Neuroscience 10, 26572668.Google Scholar
Bullier, J., Hupé, J.M., James, A.C., & Girard, P. (2001). The role of feedback connections in shaping the responses of visual cortical neurons. In Progress in Brain Research, ed. Casanova, C. & Ptito, M., pp. 193204. Netherlands: Elsevier Science B.V.
Bullier, J., McCourt, M.E., & Henry, G.H. (1988). Physiological studies on the feedback connections to the striate cortex from cortical areas 18 and 19 of the cat. Experimental Brain Research 70, 9098.Google Scholar
Cantone, G., McFarlane, N., & Levitt, J.B. (2002). Corticocortical connections among ferret visual areas. Society for Neuroscience Abstracts 28, 159.3.Google Scholar
Cantone, G., Xiao, J., & Levitt, J.B. (2003). Retinotopic organization of ferret suprasylvian cortex. Society for Neuroscience Abstracts 29, 818.9.Google Scholar
Cantone, G., Xiao, J., McFarlane, N., & Levitt, J.B. (2005). Feedback connections to ferret striate cortex: Direct evidence for visuotopic convergence of feedback inputs. Journal of Comparative Neurology 487, 312331.Google Scholar
Cavanaugh, J.R., Bair, W., & Movshon, J.A. (2002). Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. Journal of Neurophysiology 88, 25472556.Google Scholar
Clare, M.H. & Bishop, G.H. (1954). Responses from an association area secondarily activated from optic cortex. Journal of Neurophysiology 17, 271277.Google Scholar
Daniel, P.M. & Whitteridge, D. (1961). The representation of the visual field on cerebral cortex in monkeys. Journal of Physiology (Paris) 159, 203201.Google Scholar
DeAngelis, G.C., Freeman, R.D., & Ohzawa, I. (1994). Length and width tuning of neurons in the cat's primary visual cortex. Journal of Neurophysiology 71, 347374.Google Scholar
Dinse, H.R. & Krüger, K. (1994). The timing of processing along the visual pathway in the cat. Neuroreport 5, 893897.Google Scholar
Dow, B.M., Snyder, A.Z., Vautin, R.G., & Bauer, R. (1981). Magnification factor and receptive field size in foveal striate cortex of the monkey. Experimental Brain Research 44, 213228.Google Scholar
Dreher, B., Wang, C., Turlejski, K.J., Djavadian, R.L., & Burke, W. (1996). Areas PMLS and 21a of cat visual cortex: Two functionally distinct areas. Cerebral Cortex 6, 585599.Google Scholar
Fiorani, M., Gattass, R., Rosa, M.G.P., & Sousa, A.P.B., (1989). Visual area MT in the Cebus monkey: Location, visiotopic organization, and variability. Journal of Comparative Neurology 287, 98118.Google Scholar
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurology Research 1, 203209.Google Scholar
Gattass, R. & Gross, C.G. (1981). Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 621638.Google Scholar
Gattass, R., Gross, C.G., & Sandell, J.H. (1981). Visual topography of V2 in the macaque. Journal of Comparative Neurology 201, 519539.Google Scholar
Gattass, R., Sousa, A.P., & Gross, C.G. (1988). Visuotopic organization and extent of V3 and V4 of the macaque. Journal of Neuroscience 8, 18311845.Google Scholar
Gilbert, C.D. & Wiesel, T.N. (1990). The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Research 30, 16891701.Google Scholar
Grant, S. & Shipp, S. (1991). Visuotopic organization of the lateral suprasylvian area and of an adjacent area of the ectosylvian gyrus of cat cortex: A physiological and connectional study. Visual Neuroscience 6, 315338.Google Scholar
Henderson, Z. (1985). Distribution of ganglion cells in the retina of adult pigmented ferret. Brain Research 358, 221228.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1974). Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor. Journal of Comparative Neurology 158, 295306.Google Scholar
Innocenti, G.M., Manger, P., Masiello, I., Colin, I., & Tettoni, L. (2002). Architecture and callosal connections of visual areas 17, 18, 19 and 21 in the ferret (Mustella putorius). Cerebral Cortex 12, 411422.Google Scholar
Katsuyama, N., Tsumoto, T., Sato, H., Fukuda, M., & Hata, Y. (1996). Lateral suprasylvian visual cortex is activated earlier than or synchronously with primary visual cortex in the cat. Neuroscience Research 24, 431435.Google Scholar
Knierim, J.J. & Van Essen, D.C. (1992). Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. Journal of Neurophysiology 67, 961980.Google Scholar
Law, M.I., Zahs, K., & Stryker, M. (1988). Organization of primary visual cortex (area 17) in the ferret. Journal of Comparative Neurology 278, 157180.Google Scholar
Levitt, J.B. & Lund, J.S. (1997). Contrast dependence of contextual effects in primate visual cortex. Nature 387, 7376.Google Scholar
Li, C. & Li, W. (1994). Extensive integration field beyond the classic receptive field of cat's striate cortical neurons-classification and tuning properties. Vision Research 34, 23372355.Google Scholar
Maffei, R. & Fiorentini, A. (1976). The unresponsive regions of visual cortical receptive fields. Vision Research 16, 11311139.Google Scholar
Manger, P., Kiper, D., Masiello, I., Murilo, L., Tettoni, L., Hunyadi, Z., & Innocenti, G.M. (2002a). The representation of the visual field in three extrastriate areas of the ferret (Mustella putorius). Cerebral Cortex 12, 411422.Google Scholar
Manger, P., Masiello, I., & Innocenti, G.M., (2002b). Areal organization of the posterior parietal cortex of the ferret (Mustella putorius). Cerebral Cortex 12, 12801297.Google Scholar
Manger, P.R., Nakamura, H., Valentiniene, S., & Innocenti, G.M. (2004). Visual areas in the lateral temporal cortex of the ferret (Mustela putorius). Cerebral Cortex 14, 676689.Google Scholar
Maunsell, J.H. & Van Essen, D.C. (1983a). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 25632586.Google Scholar
Maunsell, J.H. & Van Essen, D.C. (1983b). Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. Journal of Neurophysiology 49, 11271147.Google Scholar
Maunsell, J.H. & Van Essen, D.C. (1987). Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries. Journal of Comparative Neurology 266, 535555.Google Scholar
Morgan, J.E., Henderson, Z., & Thompson, I.D. (1987). Retinal decussation patterns in pigmented and albino ferrets. Neuroscience 20, 519535.Google Scholar
Mulligan, K. & Sherk, H. (1993). A comparison of magnification functions in area 19 and the lateral suprasylvian visual area in the cat. Experimental Brain Research 97, 195208.Google 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, 237256.Google Scholar
Payne, B.R. (1993). Evidence for visual cortical area homologs in cat and macaque monkey. Cerebral Cortex 3, 125.Google Scholar
Philipp, R., Distler, C., & Hoffmann, K.P. (2006). A motion-sensitive area in ferret extrastriate visual cortex: An analysis in pigmented and albino animals. Cerebral Cortex, in press.Google Scholar
Pinon, M.C., Gattass, R., & Sousa, A.P. (1998). Area V4 in Cebus monkey: extent and visuotopic organization. Cerebral Cortex 8, 685701.Google Scholar
Raiguel, S.E., Lagae, L., Gulyas, B., & Orban, G.A. (1989). Response latencies of visual cells in macaque areas V1, V2 and V5. Brain Research 493, 155159.Google Scholar
Salin, P.A., Girard, P., Kennedy, H., & Bullier, J. (1992). Visuotopic organization of corticocortical connections in the visual system of the cat. Journal of Comparative Neurology 320, 415434.Google Scholar
Sanides, F. & Hoffmann, J. (1969). Cyto- and myelo-architecture of the visual cortex of the cat and of the surrounding integration cortices. Journal of Hirnforschung 11, 79104.Google Scholar
Sceniak, M.P., Hawken, M.J., & Shapley, R. (2001). Visual spatial characterization of macaque V1 neurons. Journal of Neurophysiology 85, 18731887.Google Scholar
Sengpiel, F., Sen, A., & Blakemore, C. (1997). Characteristics of surround inhibition in the cat. Experimental Brain Research 116, 216228.Google Scholar
Sherk, H. (1986). Coincidence of patchy inputs from the lateral geniculate complex and area 17 to the cat's Clare-Bishop area. Journal of Comparative Neurology 253, 105120.Google Scholar
Sherk, H. & Mulligan, K.A. (1992). Retinotopic order is surprisingly good within cell columns in the cat's lateral suprasylvian cortex. Experimental Brain Research 91, 4660.Google Scholar
Sherk, H. & Mulligan, K.A. (1993). A reassessment of the lower visual field map in striate-recipient lateral suprasylvian cortex. Visual Neuroscience 10, 131158.Google Scholar
Sherk, H. & Ombrellaro, M. (1988). The retinotopic match between area 17 and its targets in visual suprasylvian cortex. Experimental Brain Research 72, 225236.Google Scholar
Shipp, S. & Grant, S. (1991). Organization of reciprocal connections between area 17 and the lateral suprasylvian area of cat visual cortex. Visual Neuroscience 6, 339355.Google Scholar
Sillito, A.M., Grieve, K.L., Jones, H.E., Cudeiro, J., & Davis, J. (1995). Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492496.Google Scholar
Sincich, L.C., Park, K.F., Wohlgemuth, M.J., & Horton, J.C. (2004). Bypassing V1: A direct geniculate input to area MT. Nature Neuroscience 7, 11231128.Google Scholar
Spatz, W.B. (1977). Topographically organized reciprocal connections between areas 17 and MT (visual area of superior temporal sulcus) in the marmoset Callithrix jacchus. Experimental Brain Research 27, 559572.Google Scholar
Tigges, J., Spatz, W.B., & Tiggs, M. (1973). Reciprocal point-to-point connections between parastriate and striate cortex in squirrel monkey (Saimiri). Journal Comparative Neurology 148, 481490.Google Scholar
Tusa, R.J. & Palmer, L.A. (1980). Retinotopic organization of areas 20 and 21 in the cat. Journal of Comparative Neurology 193, 147164.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, 213235.Google Scholar
Tusa, R.J., Rosenquist, A.C., & Palmer, L.A. (1979). Retinotopic organization of areas18 and 19 in the cat. Journal of Comparative Neurology 185, 657678.Google Scholar
Van de Grind, W.A., Koenderink, J.J., Van Doorn, A.J., Milders, M.V., & Voerman, H. (1993). Inhomogeneity and anisotropies for motion detection in the monocular visual field of human observers. Vision Research 33, 10891107.Google Scholar
Van Essen, D.C. & Zeki, S.M. (1978). The topographical organization of rhesus monkey prestriate cortex. Journal of Physiology 277, 193226.Google Scholar
Van Essen, D.C., Maunsell, J.H., & Bixby, J.L. (1981). The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization. Journal of Comparative Neurology 199, 293326.Google Scholar
Vitek, D.J., Schall, J.D., & Leventhal, A.G. (1985). Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret. Journal of Comparative Neurology 241, 111.Google Scholar
Walker, G.A., Ohzawa, I., & Freeman, R. (1999). Asymmetric suppression outside the classic receptive field of the visual cortex. Journal of Neuroscience 19, 1053610553.Google Scholar
White, L.E., Basole, A., & Fitzpatrick, D. (2002). Functional and anatomical characterization of an extrastriate area in ferret visual cortex. Society for Neuroscience Abstracts 28, 159.5.Google Scholar
Wong-Riley, M. (1979). Reciprocal connections between striate and prestriate cortex in the squirrel monkey as demonstrated by combined peroxidase histochemistry and autoradiography. Brain Research 147, 159164.Google Scholar
Yu, H., Farley, B.J., Jin, D.Z., & Sur, M. (2005). The coordinated mapping of visual space and response features in visual cortex. Neuron 47, 267280.Google Scholar
Zeki, SM. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology 236, 549573.Google Scholar