Abstract
Prior studies suggest the presence of a color-selective area in the inferior occipital-temporal region of human visual cortex. It has been proposed that this human area is homologous to macaque area V4, which is arguably color selective, but this has never been tested directly. To test this model, we compared the location of the human color-selective region to the retinotopic area boundaries in the same subjects, using functional magnetic resonance imaging (fMRI), cortical flattening and retinotopic mapping techniques. The human color-selective region did not match the location of area V4 (neither its dorsal nor ventral subdivisions), as extrapolated from macaque maps. Instead this region coincides with a new retinotopic area that we call 'V8', which includes a distinct representation of the fovea and both upper and lower visual fields. We also tested the response to stimuli that produce color afterimages and found that these stimuli, like real colors, caused preferential activation of V8 but not V4.
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References
Cornsweet, T.N. Visual Perception (Academic Press, New York, 1970).
Judd, D.B. & Wyszecki, G. Color in Business, Science, & Industry 3rd edn 388 (Wiley, New York, 1975).
Dow, B.M. Functional classes of cells and their laminar distribution in monkey visual cortex. J. Neurophysiol. 37, 927–946 (1974).
Livingstone, M.S. & Hubel, D.H. Anatomy and physiology of a color system in the primate visual cortex. J. Neurosci. 4, 309–356 (1984).
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., De Valois, R.L. & Switkes, E. Functional anatomy of macaque striate cortex: III. Color J. Neurosci. 8, 1569–1593 (1988).
Ts'o, D.Y., Frostig, R.D., Lieke, E.E. & Grinvald, A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417–420 (1990).
Lennie, P., Krauskopf, J. & Sclar, G. Chromatic machanisms in striate cortex of macaque. J. Neurosci. 10, 649–669 ( 1990).
Leventhal, A.G., Thompson, K.G., Liu, D., Zhou, Y. & Ault, S.J. Concommitant sensitivity to orientation, direction and color of cells in layers 2, 3 and 4 of monkey striate cortex. J. Neurosci. 15, 1808–1818 (1995).
Hubel, D.H. & Livingstone, M.S. Segregation of form, color and stereopsis in primate area 18. J. Neurosci. 7, 3378–3415 (1987).
Tootell, R.B.H. & Hamilton, S.L. Functional anatomy of the second cortical visual area (V2) in the macaque. J. Neurosci. 9, 2620–2644 (1989).
Gegenfurtner, K.R., Kiper, D.C. & Fenstemaker, S.B. Processing of color, form and motion in macaque area V2. Vis. Neurosci. 13, 161– 172 (1996).
Zeki, S.M. Colour coding in rhesus monkey prestriate cortex. Brain Res. 27, 422–427 (1973).
Zeki, S.M. Colour coding in the superior temporal sulcus of rhesus monkey visual cortex. Proc. R. Soc. Lond. B 197, 195– 223 (1977).
Zeki, S. Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex . J. Physiol. (Lond.) 277, 273– 290 (1978).
Zeki, S. The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex. Proc. R. Soc. Lond. B 217, 449–470 (1983).
Schein, S.J., Marrocco, R.T. & de Monasterio, F.M. Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? J. Neurophysiol. 47, 193–213 (1982).
Heywood, C.A., Gadotti, A. & Cowey, A. Cortical area V4 and its role in the perception of color. J. Neurosci. 12, 4056–4065 (1992).
Heywood, C.A., Gaffan, D. & Cowey, A. Cerebral achromatopsia in monkeys. Eur. J. Neurosci. 7, 1064–1073 (1995).
Cowey, A. & Heywood, C.A. There's more to colour than meets the eye. Behav. Brain Res. 71, 89 –100 (1995).
Lueck, C.J. et al. The colour centre in the cerebral cortex of man. Nature 340, 386–389 (1989).
Zeki, S. et al. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11, 641–649 (1991).
McKeefry, D.J. & Zeki, S. The position and topography of the human colour centre as revealed by functional magnetic resonance imaging. Brain 120, 2229–2242 (1997).
Pearlman, A.L., Birch, J. & Meadows, J.C. Cerebral color blindness: An acquired defect in hue discrimination. Ann. Neurol. 5, 253 –261 (1979).
Damasio, A., Yamada, T., Damasio, H., Corbett, J. & McKee, J. Central achromatopsia: Behavioral, anatomic, and physiologic aspects. Neurology 30, 1064– 1071 (1980).
Zeki, S. A century of cerebral achromatopsia. Brain 113, 1721– 1777 (1990).
Tootell, R.B.H. et al. Functional analsis of V3A and related areas in human visual cortex. J. Neurosci. 17, 7076–7078 (1997).
Engel, S., Zhang, X. & Wandell, B. Colour tuning in human visual cortex measured with functional magnetic resonance imaging. Nature 388, 68– 71 (1997).
Kennard, C., Lawden, M., Morland, A.B. & Ruddock, K.H. Colour identification and colour constancy are impaired in a patient with incomplete achromatopsia associated with prestriate cortical lesions. Proc. R. Soc. Lond. B 260, 169–175 ( 1995).
Sakai, K. et al. Functional mapping of the human colour centre with echo-planar magnetic resonance imaging. Proc. R. Soc. Lond. B 261, 89–98 (1995).
Kleinschmidt, A., Lee, B.B., Requardt, M. & Frahm, J. Functional mapping of color processing by magnetic resonance imaging of responses to selective P- and M-pathway stimulation. Exp. Brain Res. 110 , 279–288 (1996).
DeYoe, E.A. et al. Mapping striate and extrastriate visual areas in human cerebral cortex. Proc. Natl. Acad. Sci. USA 93, 2382– 2386 (1996).
Sereno, M.I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889 –893 (1995).
Tootell, R.B.H., Dale, A.M., Sereno, M.I. & Malach, R. New images from human visual cortex. Trends Neurosci. 19, 481–489 (1996).
Galletti, C. Fattori, P., Battaglini, P.P., Shipp, S. & Zeki, S. Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur. J. Neurosci. 8, 30–52 (1996).
Boussaoud, D., Desimone, R. & Ungerleider, L.G. Visual topography of area TEO in the macaque. J. Comp. Neurol. 306, 554–575 (1991).
Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).
Zeki, S. Are areas TEO and PIT of monkey visual cortex wholly distinct from the fourth visual complex (V4 complex)? Proc. R. Soc. Lond. B 263, 1539–1544 (1996).
Maguire, W.M. & Baizer, J.S. Visuotopic organization of the prelunate gyrus in rhesus monkey. J. Neurosci. 7, 1690–1704 (1984).
Van Essen, D.C., Maunsell, J.H. & Bixby J.L. The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization. J. Comp. Neurol. 199, 293–326 (1981).
Tootell, R.B.H. et al. Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375, 139–141 (1995).
Tootell, R.B.H. et al. Functional analysis of primary visual cortex (V1) in humans. Proc. Natl. Acad. Sci. USA 95, 811– 817 (1998).
Craik, K.J.W. Origin of visual afterimages. Nature 145, 512 (1940).
Brindley, G.S. Two new properties of foveal afterimages and a photochemical hypothesis to explain them. J. Physiol. 164, 168–179 (1962).
Schiller, P.H. & Dolan, R.P. Visual aftereffects and the consequences of visual system lesions on their perception in the rhesus monkey. Vis. Neurosci. 11, 643–665 (1994).
Jameson, D., Hurvich, L.M. & Varner, F.D. Receptoral and postreceptoral processes in recovery from chromatic adaptation. Proc. Natl. Acad. Sci. USA 76, 3034–3038 (1979).
Tootell, R.B.H. & Taylor, J.B. Anatomical evidence for MT and additional cortical visual areas in humans. Cereb. Cortex 5, 39–55 (1995).
Tootell, R.B.H. et al. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 15, 3215–3230 (1995).
Jacobs, G.H. & Deegan, J.F. Spectral sensitivity of macaque monkeys measured with ERG flicker photometry. Vis. Neurosci. 14, 921–928 ( 1997).
DeYoe, E.A., Felleman, D.J., Van Essen, D.C. & McClendon, E. Multiple processing streams in occipitotemporal visual cortex. Nature 371, 151–154 (1994).
Engel, S.A., Glover, G.H. & Wandell, B.A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7, 181–192 (1997).
Acknowledgements
This work was supported by grants from the Human Frontiers Science Foundation and NEI EY07980 to R.B.H.T., NEI EY09258 to P.C. and Swiss Fonds National de la Recherche Scientifique to N.H. We thank Terry Campbell and Mary Foley for scanning and participation in these experiments, Robert Savoy, Ken Kwong, Bruce Fischl and Kevin Hall for advice, Tommy Vaughan for coil design and manufacture and Martin Sereno for modifying pilot stimuli. Wim Vanduffel, Ekkehardt Kustermann and Irene Tracy also helped in preliminary versions of this experiment.
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Hadjikhani, N., Liu, A., Dale, A. et al. Retinotopy and color sensitivity in human visual cortical area V8. Nat Neurosci 1, 235–241 (1998). https://doi.org/10.1038/681
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DOI: https://doi.org/10.1038/681
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