Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-16T20:00:18.140Z Has data issue: false hasContentIssue false
  • English
  • Français

Perceptual filling-in at the scotoma following a monocular retinal lesion in the monkey

Published online by Cambridge University Press:  02 June 2009

Ikuya Murakami ,
Hidehiko Komatsu  and
Masaharu Kinoshita
Ikuya Murakami
Affiliation:
Neuroscience Section, Electrotechnical Laboratory, 1-1-4 Umezono, Tsukubashi, Ibaraki 305, Japan
Hidehiko Komatsu
Affiliation:
Neuroscience Section, Electrotechnical Laboratory, 1-1-4 Umezono, Tsukubashi, Ibaraki 305, Japan
Masaharu Kinoshita
Affiliation:
Neuroscience Section, Electrotechnical Laboratory, 1-1-4 Umezono, Tsukubashi, Ibaraki 305, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

Although no visual inputs arise from the blind spot, the same visual attribute there as in the visual field surrounding the blind spot is perceived. Because of this remarkable “perceptual filling-in,” a hole corresponding to the blind spot is not perceived, even when one eye is closed. Does the same phenomenon occur in the case of a scotoma in which visual inputs are lost postnatally due to a retinal lesion? We report that it did: in the macaque monkey, behavioral evidence for filling-in at a scotoma produced by a laser-induced monocular retinal lesion was obtained. The visual receptive fields of neurons in the primary visual cortex (VI) in and around the representation of the visual field corresponding to the scotoma were also mapped, and no clear difference between the retinotopic organization of this part in VI and that found in the normal visual field was found. Also, perceptual filling-in was found to occur only two days after the lesion. These findings suggest that the normal visual system possesses a mechanism that yields filling-in when some part of the retina is damaged, and that such a mechanism requires no topographical reorganization in VI.

Keywords

Macaque monkeyScotomaPerceptual filling-inRetinal lesionsPrimary visual cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 89 - 101
Copyright
Copyright © Cambridge University Press 1997

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

Chino, Y.M., IIISmith, E.L., Kaas, J.H., Sasaki, Y. & Cheng, H. (1995). Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats. Journal of Neuroscience 15, 2417–2433.CrossRefGoogle ScholarPubMed
Chino, Y.M., Kaas, J.H., IIISmith, E.L., Langston, A.L. & Cheng, H. (1992). Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina. Vision Research 32, 789–796.CrossRefGoogle ScholarPubMed
Darian-Smith, C. & Gilbert, C.D. (1995). Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. Journal of Neuroscience 15, 1631–1647.CrossRefGoogle Scholar
De Weerd, P., Gattass, R., Desimone, R. & Ungerleider, L.G. (1995). Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma. Nature 377, 731–734.CrossRefGoogle ScholarPubMed
Fiorani, M. Jr., Rosa, M.G.P., Gattass, R. & Rocha-Miranda, C.E. (1992). Dynamic surrounds of receptive fields in primate striate cortex: A physiological basis for perceptual completion? Proceedings of the National Academy of Sciences of the U.S.A. 89, 8547–8551.CrossRefGoogle Scholar
Gerrits, H.J.M. & Vendrik, A.J.H. (1970). Simultaneous contrast, filling-in process and information processing in man's visual system. Experimental Brain Research 11, 411–430.CrossRefGoogle ScholarPubMed
Gerrits, H.J.M.G. & Timmerman, G.J.M.E.N. (1969). The filling-in process in patients with retinal scotomata. Vision Research 9, 439–442.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1992). Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152.CrossRefGoogle ScholarPubMed
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coil for measurement of eye position: An improved method. Vision Research 20, 535–538.CrossRefGoogle Scholar
Kaas, J.H., Krubitzer, L.A., Chino, Y.M., Langston, A.L., Polley, E.H. & Blair, N. (1990). Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229–231.CrossRefGoogle ScholarPubMed
Kinoshita, M., Murakami, I., Kimura, T. & Komatsu, H. (1994). Perceptual filling-in at monocular scotoma does not require reorganization of the retinotopic map of the monkey V1. Neuroscience Research (Suppl.) 19, S203.Google Scholar
Kinoshita, M., Murakami, I., Kimura, T. & Komatsu, H. (1995). Perceptual filling-in occurs at the monocular scotoma without reorganization of retinotopic map of the monkey VI. Fourth IBRO World Congress of Neuroscience Abstracts 282.Google Scholar
Komatsu, H. & Ideura, Y. (1993). Relationships between color, shape, and pattern selectivities of neurons in the inferior temporal cortex of the monkey. Journal of Neurophysiology 70, 677–694.CrossRefGoogle ScholarPubMed
Komatsu, H. & Murakami, I. (1994 a). Behavioral evidence of filling-in at the blind spot of the monkey. Visual Neuroscience 11, 1103–1113.CrossRefGoogle ScholarPubMed
Komatsu, H. & Murakami, I. (1994 b). Huge receptive fields of the neurons in the retinotopic map of the macaque VI representing the blind spot. Neuroscience Research (Suppl.) 19, S199.Google Scholar
Komatsu, H., Murakami, I. & Kinoshita, M. (1995). Spatial summation properties of the macaque VI neurons in the retinotopic representation of the blind spot. Society for Neuroscience Abstracts 21, 1648.Google Scholar
Levay, S., Connolly, M., Houde, J. & Van Essen, D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience 5, 486–501.CrossRefGoogle ScholarPubMed
Murakami, I. (1995). Motion aftereffect after monocular adaptation to filled-in motion at the blind spot. Vision Research 35, 1041–1045.CrossRefGoogle ScholarPubMed
Murakami, I., Kinoshita, M., Kimura, T. & Komatsu, H. (1995). Do VI neurons representing the blind spot region respond to stimuli for perceptual filling-in? Fourth IBRO World Congress of Neuroscience Abstracts 282.Google Scholar
Murakami, I. & Komatsu, H. (1993). Filling-in at an artificial scotoma of the monkey: Behavioral evidence. Neuroscience Research (Suppl.) 18, S187.Google Scholar
Ramachandran, V.S. (1992 a). The blind spot. Scientific American 266, 86–91.CrossRefGoogle Scholar
Ramachandran, V.S. (1992 b). Perceptual “filling in” of the blind spot and of cortical and retinal scotomas. Investigative Ophthalmology and Visual Science 33, 1348.Google Scholar
Ramachandran, V.S. & Gregory, R.L. (1991). Perceptual filling in of artificially induced scotomas in human vision. Nature 350, 699–702.CrossRefGoogle ScholarPubMed
Ramachandran, V.S., Gregory, R.L. & Aiken, W. (1993). Perceptual fading of visual texture borders. Vision Research 33, 717–721.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions on Biomedical Electronics 10, 137–145.Google ScholarPubMed
Schmid, L.M., Rosa, M.G.P. & Calford, M.B. (1995). Retinal detachment induces massive immediate reorganization in visual cortex. Neuroreport 6, 1349–1353.CrossRefGoogle ScholarPubMed
Schmid, L.M., Rosa, M.G.P., Calford, M.B. & Ambler, J.S. (1996). Visuotopic reorganization in the primary visual cortex of adult cats following monocular and binocular retinal lesions. Cerebral Cortex 6, 388–405.CrossRefGoogle ScholarPubMed
Todorovic, D. (1987). The Craik-O'Brien-Cornsweet effect: New varieties and their theoretical implications. Perception and Psychophysics 42, 545–560.CrossRefGoogle ScholarPubMed
Tripathy, S.P. & Levi, D.M. (1994). Long-range dichoptic interactions in the human visual cortex in the region corresponding to the blind spot. Vision Research 34, 1127–1138.CrossRefGoogle Scholar
Tripathy, S.P. & Levi, D.M. (1995). Long-range dichoptic interactions in human vision around a pathological retinal scotoma. Journal of Physiology 485P, 27–28.Google Scholar
Tripathy, S.P., Levi, D.M., Ogmen, H. & Harden, C. (1995). Perceived length across the physiological blind spot. Visual Neuroscience 12, 385–402.CrossRefGoogle ScholarPubMed
Troxler, D. (1804). Ueber das Verschwinden gegebener Gegenstände innerhalb unseres Gesichtskreises. In Ophthalmische Bibliothek, 2, eds. Himly, K. & Schmidt, J.A., pp. 51–53. Jena: Fromann.Google Scholar
Van Essen, D.C., Newsome, W.T. & Maunsell, J.H.R. (1984). The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability. Vision Research 24, 429–448.CrossRefGoogle ScholarPubMed
Walls, G.L. (1954). The filling-in process. American Journal of Optometry and Archives of American Academy of Optometry 31, 329–341.CrossRefGoogle ScholarPubMed