Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-22T20:15:22.714Z Has data issue: false hasContentIssue false
  • English
  • Français

Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques

Published online by Cambridge University Press:  02 June 2009

Peter De Weerd ,
Robert Desimone  and
Leslie G. Ungerleider
Peter De Weerd
Affiliation:
Laboratory of Psychology and Psychopathology, NIMH, Bethesda
Robert Desimone
Affiliation:
Laboratory of Neuropsychology, NIMH, Bethesda
Leslie G. Ungerleider
Affiliation:
Laboratory of Psychology and Psychopathology, NIMH, Bethesda
Get access Rights & Permissions [Opens in a new window]

Abstract

To examine the role of visual area V4 in pattern vision, we tested two monkeys with lesions of V4 on tasks that required them to discriminate the orientation of contours defined by several different cues. The cues used to separate the contours from their background included luminance, color, motion, and texture, as well as phase-shifted abutting gratings that created an “illusory” contour. The monkeys were trained to maintain fixation on a fixation target while discriminating extrafoveal stimuli, which were located in either a normal control quadrant of the visual field or in a quadrant affected by a lesion of area V4 in one hemisphere. Comparing performance in the two quadrants, we found significant deficits for contours defined by texture and for the illusory contour, but smaller or no deficits for motion-, color-, and luminance-defined contours. The data suggest a specific role of V4 in the perception of illusory contours and contours defined by texture.

Keywords

MacaqueArea V4Lesion effectsTexture-defined contoursIllusory contour
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 3 , May 1996 , pp. 529 - 538
Copyright
Copyright © Cambridge University Press 1996

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

Baizer, J.S., Ungerleider, L.G., & Desimone, R. (1991). Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. Journal of Neitroscience 11, 168–190.Google Scholar
Boussaoud, D., Desimone, R., & Ungerleider, L.G. (1991). Visual topography of area TEO in the macaque. Journal of Comparative Neurology 306, 554–575.CrossRefGoogle ScholarPubMed
Britten, K.H., Newsome, W.T., & Saunders, R.C. (1992). Effects of inferotemporal lesions on form-from-motion discrimination in monkeys. Experimental Brain Research 88, 292–302.CrossRefGoogle ScholarPubMed
Cowey, A. & Gross, C.G. (1970). Effects of foveal prestriate and infero-temporal lesions on visual discrimination by rhesus monkeys. Experimental Brain Research 11, 128–144.CrossRefGoogle Scholar
Creutzfeldt, O.D., Weber, H., Tanaka, M., & Lee, B.B. (1987). Neuronal representation of spectral and spatial stimulus aspects in foveal and parafoveal area 17 of the awake monkey. Experimental Brain Research 68, 541–564.CrossRefGoogle ScholarPubMed
Desimone, R., Fleming, J., & Gross, C.G. (1980). Prestriate afferents to inferior temporal cortex: an HRP study. Brain Research 184, 41–55.CrossRefGoogle ScholarPubMed
Desimone, R. & Schein, S.J. (1987). Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. Journal of Neurophysiology 57, 835–868.CrossRefGoogle ScholarPubMed
Desimone, R., Li., L., Lehky, S., Ungerleider, L.G., & Mishkin, M. (1990). Effects of V4 lesions on visual discrimination performance and on responses of neurons in inferior temporal cortex. Society for Neuroscience Abstracts 16, 621.Google Scholar
Desimone, R., Schein, S.J., Moran, J., & Ungerleider, L.G. (1985). Contour, color and shape analysis beyond the striate cortex. Vision Research 25, 441–452.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1989). Neural mechanisms of visual processing in monkeys. In Handbook of Neuropsychology, Vol 2, ed. Boller, F. & Grafman, J., pp. 267–299, Amsterdam: Elsevier, Science Publishers B.V. (Biomedical Division).Google Scholar
De Weerd, P., Sprague, J.M., Raiguel, S., Vandenbussche, E., & Orban, G.A. (1993 a). Effects of visual cortex lesions on orientation discrimination of illusory contours in the cat. European Journal of Neuroscience 5, 1695–1710.CrossRefGoogle ScholarPubMed
De Weerd, P., Vandenbussche, E., & Orban, G.A. (1993 b). Occlusion cues contribute to orientation judgments of occlusion-defined contours. Perception and Psychophysics 54, 706–715.CrossRefGoogle ScholarPubMed
De Weerd, P., Sprague, J.M., Raiguel, S., Vandenbussche, E., & Orban, G.A. (1994). Two stages in visual texture segregation: A lesion study in the cat. Journal of Neuroscience 14, 929–948.CrossRefGoogle ScholarPubMed
Deyoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317, 58–61.CrossRefGoogle ScholarPubMed
Distler, C., Boussaoud, D., Desimone, R., & Ungerleider, L.G. (1993). Cortical connections of inferior temporal area TEO in macaque monkeys. Journal of Comparative Neurology 334, 125–150.CrossRefGoogle ScholarPubMed
Gallant, J.L., Braun, J., & Van Essen, D.C. (1993). Selectivity for polar, hyperbolic and Cartesian gratings in macaque visual cortex. Science 259, 100–103.CrossRefGoogle ScholarPubMed
Gattass, R. & Gross, C.G. (1981). Visual topography of the striate projection zone (MT) in posterior superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 621–638.CrossRefGoogle ScholarPubMed
Gattass, R., Rosa, M.G.P., Sousa, M.P.B., Pinon, M.C.G., Fiorani, M. Jr., & Neuenschwander, S. (1990). Cortical streams of visual information processing in primates. Brazilian Journal of Medical and Biological Research 23, 375–393.Google ScholarPubMed
Gattass, R., Sousa, A.P.B., & Gross, C.G. (1988). Visuotopic organization and extent of V3 and V4 of the macaque. Journal of Neuroscience 8, 1831–1845.CrossRefGoogle ScholarPubMed
Gouras, P. (1974). Neuronal representation of spectral and spatial stimulus aspects in foveal and parafoveal area 17 of the awake monkey. Experimental Brain Research 68, 541–564.Google Scholar
Grosof, D.H., Shapley, R.M., & Hawken, R.M. (1993). Macaque VI neurons can signal ‘illusory’ contours. Nature 365, 550–552.CrossRefGoogle Scholar
Grossberg, S. (1994). 3-D vision and figure-ground separation by visual cortex. Perception and Psychophysics 55, 48–120.CrossRefGoogle ScholarPubMed
Heywood, C.A. & Cowey, A. (1987). On the role of cortical area V4 in the discrimination of hue and pattern in macaque monkeys. Journal of Neuroscience 7, 2601–2617.CrossRefGoogle ScholarPubMed
Heywood, C.A., Gadotti, A., & Cowey, A. (1992). Cortical area V4 and its role in the perception of color. Journal of Neuroscience 12, 4056–4065.CrossRefGoogle ScholarPubMed
Iversen, S.D. (1973). Visual discrimination deficits associated with posterior inferotemporal lesions in the monkey. Brain Research 62, 89–101.CrossRefGoogle ScholarPubMed
Iwai, E. (1985). Neurophysiological basis of pattern vision in macaque monkeys. Vision Research 25, 425–439.CrossRefGoogle Scholar
Iwai, E. & Mishkin, M. (1969). Further evidence on the locus of the visual area in the temporal lobe of the monkey. Experimental Neurology 25, 585–594.CrossRefGoogle ScholarPubMed
Kikuchi, R. & Iwai, E. (1980). The locus of the posterior subdivision of the inferotemporal visual learning area in the monkey. Brain Research 198, 347–360.CrossRefGoogle ScholarPubMed
Knierim, J.J. & Van Essen, D.C. (1992). Neuronal responses to static texture patterns in area VI of the alert macaque monkey. Journal of Neurophysiology 67, 961–980.CrossRefGoogle Scholar
Kobatake, E. & Tanaka, K. (1994). Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. Journal of Neurophysiology 71, 856–867.CrossRefGoogle ScholarPubMed
Krubitzer, L. & Kaas, J. (1990). Convergence of processing channels in the extrastriale cortex of monkeys. Visual Neuroscience 5, 609–613.CrossRefGoogle ScholarPubMed
Lamme, V.A.F. (1994). The neurophysiology of figure-ground segregation in primary visual cortex. Journal of Neuroscience 15, 1605–1615.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–365.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1987). Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey. Journal of Neuroscience 1, 3371–3377.CrossRefGoogle Scholar
Marcar, V.L., Raiguel, S.E., Maes, H., & Orban, G.A. (1991). Do cells in area MT code the orientation of a kinetic boundary? Society for Neuroscience Abstracts 17, 525.Google Scholar
Marcar, V.L., Raiguel, S.E., Xiao, D., Maes, H., & Orban, G.A. (1992). Do cells in area V2 respond to the orientation of kinetic boundaries? Society for Neuroscience Abstracts 18, 1275.Google Scholar
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
Merigan, W.H. (1996). Basic visual capabilities and shape discrimination after lesions of extrastriate area V4 in macaques. Visual Neuroscience 13, 51–60.CrossRefGoogle ScholarPubMed
Merigan, W.H., Nealy, T.A., & Maunsell, J.H.R. (1993). Visual effects of lesions of cortical area V2 in macaques. Journal of Neuroscience 13, 3180–3191.CrossRefGoogle ScholarPubMed
Mishkin, M. & Appenzeller, T. (1987). The anatomy of memory. Scientific American 256, 80–89.CrossRefGoogle ScholarPubMed
Mishkin, M., Ungerleider, L.G., & Macro, K.A. (1983). Object vision and spatial vision: two cortical pathways. Trends in Neuroscience 6, 414–417.CrossRefGoogle Scholar
Morel, A. & Bullier, J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555–578.CrossRefGoogle ScholarPubMed
Nakamura, H., Gattass, R., Desimone, R., & Ungerleider, L.G. (1993). The modular organization of projections from areas VI and V2 to areas V4 and TEO in macaques. Journal of Neuroscience 13, 3681–3691.CrossRefGoogle Scholar
Nakayama, K., Shimojo, S., & Ramachandran, V.S. (1990). Transparency: Relation to depth, subjective contours, luminance, and neon color spreading. Perception 19, 497–513.CrossRefGoogle ScholarPubMed
Nakayama, K., Shimojo, S., & Silverman, G.H. (1989). Stereoscopic depth: its relation to image segmentation, grouping, and the recognition of occluded objects. Perception 18, 55–68.CrossRefGoogle ScholarPubMed
Nelson, J.I., Salin, P.A., Munk, M.H.J., Arzi, M., & Bullier, J. (1992). Spatial and temporal coherence in cortico-cortical connections: A cross-correlation study in area 17 and area 18 in the cat. Visual Neuroscience 9, 21–37.CrossRefGoogle ScholarPubMed
Peterhans, E. & Von Der Heydt, R. (1989). Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps. Journal of Neuroscience 9, 1749–1763.CrossRefGoogle ScholarPubMed
Peterhans, E. & Von Der Heydt, R. (1993). Functional organization of area V2 in the alert monkey. European Journal of Neuroscience 5, 509–524.CrossRefGoogle Scholar
Phillips, R.R., Malamut, B.L., Bachevalier, J., & Mishkin, M. (1988). Dissociation of the effects of inferior temporal and limbic lesions on object discrimination with 24-h intertrial intervals. Behavioural Brain Research 27, 99–107.CrossRefGoogle ScholarPubMed
Reynolds, R.I. (1981). Perception of an illusory contour as a function of processing time. Perception 10, 107–115.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions of Biomedical Engineering 101, 137–145.Google Scholar
Rock, I. & Anson, R. (1979). Illusory contours as a solution to a problem. Perception 8, 665–681.CrossRefGoogle ScholarPubMed
Rosene, D.L., Roy, N.J., & Davis, B.J. (1986). A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. Journal of Histochemistry and Cytochemistry 34, 1301–1315.CrossRefGoogle ScholarPubMed
Sary, G., Vogels, R., & Orban, G.A. (1993). Cue-invariant shape selectivity of macaque inferior temporal neurons. Science 260, 995–997.CrossRefGoogle ScholarPubMed
Schein, S.J. & Desimone, R. (1990). Spectral properties of V4 neurons of the macaque. Journal of Neuroscience 10, 3369–3389.CrossRefGoogle ScholarPubMed
Schiller, P.H. (1993). The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey. Visual Neuroscience 10, 717–746.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Lee, K. (1991). The role of the primate extrastriate area V4 in vision. Science 251, 1251–1253.CrossRefGoogle ScholarPubMed
Squire, L.R. (1988). Memory and Brain. New York: Oxford University Press.Google Scholar
Thorell, L.G., De Valois, R.L., & Albrecht, D.G. (1984). Spatial mapping of monkey VI cells with pure color and luminance stimuli. Vision Research 24, 751–769.CrossRefGoogle Scholar
Tootell, R.B.H., Silverman, M.S., De Valois, R.L., & Jacobs, G.H. (1983). Functional organization of the second cortical visual area in primates. Science 220, 737–739.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. (1985). Thecorticocortical pathways for object recognition and spatial perception. In Pattern Recognition Mechanisms, Vol. 54, ed. Chagas, C., Gattass, R., & Gross, C., pp. 21–37. Vatican City, Italy: Pontificae Academiae Scientiarum Scripta Varia.CrossRefGoogle Scholar
Ungerleider, L.G. & Desimone, R. (1986). Cortical projections of visual area MT in the macaque. Journal of Comparative Neurology T.W, 248, 190–222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two visual systems. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A., & Mansfield, M.A., pp. 549–586. Cambridge: MIT Press.Google Scholar
Van Essen, D.C. (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3, ed. Jones, E.G. & Peters, A.A., pp. 259–329. New York: Plenum Press.Google Scholar
Von Der Heydt, R. & Peterhans, E. (1989). Mechanisms of contour perception in monkey visual cortex. 1. Lines of pattern discontinuity. Journal of Neuroscience 9, 1731–1748.CrossRefGoogle Scholar
Von Der Heydt, R., Peterbans, E., & Baumgartner, G. (1984). Illusory contours and cortical neuron responses. Science 224, 1260–1262.CrossRefGoogle ScholarPubMed
Walsh, V., Butler, S.R., Garden, D., & Kulikowski, J.J. (1992). The effects of V4 lesions on the visual abilities of macaques: shape discrimination. Behavioural Brain Research 52, 81–89.CrossRefGoogle Scholar
Walsh, V., Garden, D., Butler, S.R., & Kulikowski, J.J. (1993). The effects of V4 lesions on the visual abilities of macaques: Hue discrimination and colour constancy. Behavioural Brain Research 53, 51–62.CrossRefGoogle ScholarPubMed
Webster, M.J., Bachevalier, J., & Ungerleider, L.G. (1994). Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cerebral Cortex 4, 470–483.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1983). Retinotopic patterns of connections of area 17 with visual areas V-ll and MT in macaque monkeys. Journal of Comparative Neurology 220, 253–279.CrossRefGoogle Scholar
Wild, H.M., Butler, S.R., Garden, D., & Kulikowski, J.J. (1985). Primate cortical area V4 important for colour constancy but not wavelength discrimination. Nature 313, 133–135.CrossRefGoogle Scholar
Zeki, S.M. (1969). Representation of central visual fields in prestriate cortex of monkey. Brain Research 14, 271–291.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1971). Cortical projections from two striate areas in the monkey. Brain Research 34, 19–35.CrossRefGoogle Scholar
Zeki, S.M. (1978). Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. Journal of Physiology (London) 277, 273–290.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1980). The representation of colours in the cerebral cortex. Nature (London) 284, 412–418.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1983). Colour coding in the cerebral cortex: The responses of wavelength-sensitive and colour-coded cells in monkey visual cortex to changes in wavelength composition. Neuroscience 9, 767–781.CrossRefGoogle Scholar