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Color signals through dorsal and ventral visual pathways

Published online by Cambridge University Press:  08 October 2013

BEVIL R. CONWAY
BEVIL R. CONWAY*
Affiliation:
Neuroscience Program, Wellesley College, Wellesley, Massachusetts
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Abstract

Explanations for color phenomena are often sought in the retina, lateral geniculate nucleus, and V1, yet it is becoming increasingly clear that a complete account will take us further along the visual-processing pathway. Working out which areas are involved is not trivial. Responses to S-cone activation are often assumed to indicate that an area or neuron is involved in color perception. However, work tracing S-cone signals into extrastriate cortex has challenged this assumption: S-cone responses have been found in brain regions, such as the middle temporal (MT) motion area, not thought to play a major role in color perception. Here, we review the processing of S-cone signals across cortex and present original data on S-cone responses measured with fMRI in alert macaque, focusing on one area in which S-cone signals seem likely to contribute to color (V4/posterior inferior temporal cortex) and on one area in which S signals are unlikely to play a role in color (MT). We advance a hypothesis that the S-cone signals in color-computing areas are required to achieve a balanced neural representation of perceptual color space, whereas those in noncolor-areas provide a cue to illumination (not luminance) and confer sensitivity to the chromatic contrast generated by natural daylight (shadows, illuminated by ambient sky, surrounded by direct sunlight). This sensitivity would facilitate the extraction of shape-from-shadow signals to benefit global scene analysis and motion perception.

Keywords

MacaqueExtrastriateColorV4S coneinferior temporal cortex (IT)

Information

Type
Review Articles
Information
Visual Neuroscience , Volume 31 , Issue 2: Short Wavelength-Sensitive Cones and the Processing of Their Signals , March 2014 , pp. 197 - 209
Copyright
Copyright © Cambridge University Press 2013 

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References

Barberini, C.L., Cohen, M.R., Wandell, B.A. & Newsome, W.T. (2005). Cone signal interactions in direction-selective neurons in the middle temporal visual area (MT). Journal of Vision 5, 603–621.CrossRefGoogle ScholarPubMed
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1987). Spectral sensitivity of cones of the monkey macaca fascicularis. The Journal of Physiology 390, 145–160.Google Scholar
Brainard, D.H. & Stockman, A. (2010). Colorimetry. In The OSA Handbook of Optics (3rd ed.) ed. Bass, M., pp. 10.11–11.56. New York: McGraw-Hill.Google Scholar
Brouwer, G.J. & Heeger, D.J. (2009). Decoding and reconstructing color from responses in human visual cortex. The Journal of Neuroscience 29, 13992–14003.Google Scholar
Calkins, D.J., Tsukamoto, Y. & Sterling, P. (1998). Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. The Journal of Neuroscience 18, 3373–3385.Google Scholar
Cavanagh, P. (2009). All’s jazzy and unstable on the colour front: The impact of Gregory’s pioneering paper on vision at equiluminance. Perception 38, 831–832. discussion 836.Google Scholar
Chatterjee, S. & Callaway, E.M. (2002). S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35, 1135–1146.CrossRefGoogle Scholar
Conway, B.R. (2001). Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1). The Journal of Neuroscience 21, 2768–2783.Google Scholar
Conway, B.R. (2009). Color vision, cones, and color-coding in the cortex. The Neuroscientist 15, 274–290.Google Scholar
Conway, B.R., Chatterjee, S., Field, G.D., Horwitz, G.D., Johnson, E.N., Koida, K. & Mancuso, K. (2010). Advances in color science: From retina to behavior. The Journal of Neuroscience 30, 14955–14963.Google Scholar
Conway, B.R., Hubel, D.H. & Livingstone, M.S. (2002). Color contrast in macaque V1. Cerebral Cortex 12, 915–925.Google Scholar
Conway, B.R. & Livingstone, M.S. (2005). A different point of hue. Proceedings of the National Academy of Sciences of the United States of America 102, 10761–10762.Google Scholar
Conway, B.R. & Livingstone, M.S. (2006). Spatial and temporal properties of cone signals in alert macaque primary visual cortex. The Journal of Neuroscience 26, 10826–10846.Google Scholar
Conway, B.R., Moeller, S. & Tsao, D.Y. (2007). Specialized color modules in macaque extrastriate cortex. Neuron 56, 560–573.Google Scholar
Conway, B.R. & Stoughton, C.M. (2009). Towards a neural representation for unique hues. Current Biology: CB 19, R442–R443.Google Scholar
Conway, B.R. & Tsao, D.Y. (2006). Color architecture in alert macaque cortex revealed by FMRI. Cerebral Cortex 16, 1604–1613.CrossRefGoogle ScholarPubMed
Conway, B.R. & Tsao, D.Y. (2009). Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex. Proceedings of the National Academy of Sciences of the United States of America 106, 18034–18039.CrossRefGoogle ScholarPubMed
Cottaris, N.P. & De Valois, R.L. (1998). Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 395, 896–900.Google Scholar
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. The Journal of Comparative Neurology 292, 497–523.Google Scholar
D’Souza, D.V., Auer, T., Strasburger, H., Frahm, J. & Lee, B.B. (2011). Temporal frequency and chromatic processing in humans: An fMRI study of the cortical visual areas. Journal of Vision 11, 1–7.Google ScholarPubMed
Dacey, D.M. (1996). Circuitry for color coding in the primate retina. Proceedings of the National Academy of Sciences of the United States of America 93, 582–588.Google Scholar
Dacey, D.M., Crook, J.D. & Packer, O.S. (2013). Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina. Visual Neuroscience, 1–13. doi: 10.1017/S0952523813000230Google ScholarPubMed
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.Google Scholar
De Valois, R.L. & De Valois, K.K. (1993). A multi-stage color model. Vision Research 33, 1053–1065.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. The Journal of Physiology 357, 241–265.Google Scholar
DiCarlo, J.J., Zoccolan, D. & Rust, N.C. (2012). How does the brain solve visual object recognition? Neuron 73, 415–434.Google Scholar
Dobkins, K.R. & Albright, T.D. (1993). What happens if it changes color when it moves?: Psychophysical experiments on the nature of chromatic input to motion detectors. Vision Research 33, 1019–1036.CrossRefGoogle ScholarPubMed
Dobkins, K.R. & Albright, T.D. (1994). What happens if it changes color when it moves?: The nature of chromatic input to macaque visual area MT. The Journal of Neuroscience 14, 4854–4870.CrossRefGoogle ScholarPubMed
Dougherty, R.F., Press, W.A. & Wandell, B.A. (1999). Perceived speed of colored stimuli. Neuron 24, 893–899.Google Scholar
Engel, S., Zhang, X. & Wandell, B. (1997). Colour tuning in human visual cortex measured with functional magnetic resonance imaging. Nature 388, 68–71.Google Scholar
Forte, J.D., Blessing, E.M., Buzas, P. & Martin, P.R. (2006). Contribution of chromatic aberrations to color signals in the primate visual system. Journal of Vision 6, 97–105.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R. & Kiper, D.C. (2003). Color vision. Annual Review of Neuroscience 26, 181–206.Google Scholar
Gegenfurtner, K.R., Kiper, D.C., Beusmans, J.M., Carandini, M., Zaidi, Q. & Movshon, J.A. (1994). Chromatic properties of neurons in macaque MT. Visual Neuroscience 11, 455–466.Google Scholar
Ghose, G.M. & Ts’o, D.Y. (1997). Form processing modules in primate area V4. Journal of Neurophysiology 77, 2191–2196.Google Scholar
Goddard, E., Mannion, D.J., McDonald, J.S., Solomon, S.G. & Clifford, C.W. (2010). Combination of subcortical color channels in human visual cortex. Journal of Vision 10, 25.Google Scholar
Gouras, P. & Eggers, H. (1984). Hering’s opponent colour channels do not exist in the primate retinogeniculate pathway. Ophthalmic Research 16, 31–35.CrossRefGoogle Scholar
Gregory, R.L. (1977). Vision with isoluminant colour contrast: 1. A projection technique and observations. Perception 6, 113–119.Google Scholar
Gregory, R.L. & Heard, P.F. (1983). Visual dissociations of movement, position, and stereo depth: Some phenomenal phenomena. Quarterly Journal of Experimental Psychology. A 35, 217–237.CrossRefGoogle ScholarPubMed
Harada, T., Goda, N., Ogawa, T., Ito, M., Toyoda, H., Sadato, N. & Komatsu, H. (2009). Distribution of colour-selective activity in the monkey inferior temporal cortex revealed by functional magnetic resonance imaging. The European Journal of Neuroscience 30, 1960–1970.CrossRefGoogle ScholarPubMed
Horwitz, G.D. & Hass, C.A. (2012). Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing. Nature Neuroscience 15, 913–919.Google Scholar
Hubel, D. & Livingstone, M. (1990). Color puzzles. Cold Spring Harbor Symposia on Quantitative Biology 55, 643–649.Google Scholar
Ingling, C.R. Jr. (1977). The spectral sensitivity of the opponent-color channels. Vision Research 17, 1083–1089.Google Scholar
Jayakumar, J., Roy, S., Dreher, B., Martin, P.R. & Vidyasagar, T.R. (2013). Multiple pathways carry signals from short-wavelength-sensitive (‘blue’) cones to the middle temporal area of the macaque. J Physiol 591, 339–352.Google Scholar
Johnson, E.N., Hawken, M.J. & Shapley, R. (2001). The spatial transformation of color in the primary visual cortex of the macaque monkey. Nature Neuroscience 4, 409–416.Google Scholar
Johnson, E.N., Hawken, M.J. & Shapley, R. (2004). Cone inputs in macaque primary visual cortex. Journal of Neurophysiology 91, 2501–2514.Google Scholar
Johnson, E.N., Hawken, M.J. & Shapley, R. (2008). The orientation selectivity of color-responsive neurons in macaque V1. The Journal of Neuroscience 28, 8096–8106.Google Scholar
Katsuyama, N., Imamura, K., Onoe, H., Tanaka, H.K., Onoe, K., Tsukada, H. & Watanabe, Y. (2010). Cortical activation during color discrimination task in macaques as revealed by positron emission tomography. Neuroscience Letters 484, 168–173.CrossRefGoogle ScholarPubMed
Klug, K., Herr, S., Ngo, I.T., Sterling, P. & Schein, S. (2003). Macaque retina contains an S-cone OFF midget pathway. The Journal of Neuroscience 23, 9881–9887.Google Scholar
Koida, K. & Komatsu, H. (2007). Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex. Nature Neuroscience 10, 108–116.Google Scholar
Komatsu, H., Ideura, Y., Kaji, S. & Yamane, S. (1992). Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey. The Journal of Neuroscience 12, 408–424.CrossRefGoogle ScholarPubMed
Krauskopf, J., Williams, D.R. & Heeley, D.W. (1982). Cardinal directions of color space. Vision Research 22, 1123–1131.Google Scholar
Krauskopf, J., Williams, D.R., Mandler, M.B. & Brown, A.M. (1986). Higher order color mechanisms. Vision Research 26, 23–32.Google Scholar
Kravitz, D.J., Saleem, K.S., Baker, C.I. & Mishkin, M. (2011). A new neural framework for visuospatial processing. Nature Reviews. Neuroscience 12, 217–230.Google Scholar
Kravitz, D.J., Saleem, K.S., Baker, C.I., Ungerleider, L.G. & Mishkin, M. (2012). The ventral visual pathway: An expanded neural framework for the processing of object quality. Trends in Cognitive Sciences 17, 26–49.Google Scholar
Lafer-Sousa, R., Liu, Y.O., Lafer-Sousa, L., Wiest, M.C. & Conway, B.R. (2012). Color tuning in alert macaque V1 assessed with fMRI and single-unit recording shows a bias toward daylight colors. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 29, 657–670.Google Scholar
Lafer-Sousa, R. & Conway, B.R. (2013). Parallel, multi-stage processing of colors, faces, and shapes in macaque inferior temporal cortex. Nature Neuroscience in pressGoogle Scholar
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. The Journal of Neuroscience 10, 649–669.Google Scholar
Lennie, P. & Movshon, J.A. (2005). Coding of color and form in the geniculostriate visual pathway (invited review). Journal of the Optical Society of America. A, Optics, Image Science, and Vision 22, 2013–2033.Google Scholar
Liu, J. & Wandell, B.A. (2005). Specializations for chromatic and temporal signals in human visual cortex. The Journal of Neuroscience 25, 3459–3468.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. The Journal of Neuroscience 4, 309–356.Google Scholar
Lueck, C.J., Zeki, S., Friston, K.J., Deiber, M.P., Cope, P., Cunningham, V.J., Lammertsma, A.A., Kennard, C. & Frackowiak, R.S. (1989). The colour centre in the cerebral cortex of man. Nature 340, 386–389.Google Scholar
MacLeod, D.I. & Boynton, R.M. (1979). Chromaticity diagram showing cone excitation by stimuli of equal luminance. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 69, 1183–1186.Google Scholar
Martin, P.R., White, A.J., Goodchild, A.K., Wilder, H.D. & Sefton, A.E. (1997). Evidence that blue-on cells are part of the third geniculocortical pathway in primates. The European Journal of Neuroscience 9, 1536–1541.Google Scholar
Matsumora, T., Koida, K. & Komatsu, H. (2008). Relationship between color discrimination and neural responses in the inferior temporal cortex of the monkey. Journal of Neurophysiology 100, 3361–3374.Google Scholar
Mollon, J.D. (2009). A neural basis for unique hues? Current Biology: CB 19, R441–R442.Google Scholar
Moutoussis, K. & Zeki, S. (2002). Responses of spectrally selective cells in macaque area V2 to wavelengths and colors. Journal of Neurophysiology 87, 2104–2112.CrossRefGoogle ScholarPubMed
Mullen, K.T., Dumoulin, S.O. & Hess, R.F. (2008). Color responses of the human lateral geniculate nucleus: [corrected] selective amplification of S-cone signals between the lateral geniculate nucleno and primary visual cortex measured with high-field fMRI. The European Journal of Neuroscience 28, 1911–1923.Google Scholar
Mullen, K.T., Thompson, B. & Hess, R.F. (2010). Responses of the human visual cortex and LGN to achromatic and chromatic temporal modulations: An fMRI study. Journal of Vision 10, 13.Google Scholar
Munsell, A.H. (1907). A Color Notation, A Measured Color System, Based on the Three Qualities Hue, Value, and Chroma (2nd ed.) Boston: Geo. H. Ellis Co.Google Scholar
Parraga, C.A., Troscianko, T. & Tolhurst, D.J. (2002). Spatiochromatic properties of natural images and human vision. Current Biology: CB 12, 483–487.CrossRefGoogle ScholarPubMed
Percival, K.A., Jusuf, P.R., Martin, P.R. & Grunert, U. (2009). Synaptic inputs onto small bistratified (blue-ON/yellow-OFF) ganglion cells in marmoset retina. The Journal of Comparative Neurology 517, 655–669.Google Scholar
Reid, C.R. & Hendry, S.H.C. (2000). The koniocellular pathway in primate vision. Annual Review of Neuroscience 23, 127–153.Google Scholar
Reid, R.C. & Shapley, R.M. (2002). Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. The Journal of Neuroscience 22, 6158–6175.Google Scholar
Riecansky, I., Thiele, A., Distler, C. & Hoffmann, K.P. (2005). Chromatic sensitivity of neurones in area MT of the anaesthetised macaque monkey compared to human motion perception. Experimental Brain Research 167, 504–525.Google Scholar
Roe, A.W., Chelazzi, L., Connor, C.E., Conway, B.R., Fujita, I., Gallant, J., Lu, H.D. & Vanduffel, W. (2012). Towards a unified theory of visual area V4. Neuron 74, 12–29.Google Scholar
Romney, A.K. & D’Andrade, R.G. (2005). Modeling lateral geniculate nucleus cell response spectra and Munsell reflectance spectra with cone sensitivity curves. Proceedings of the National Academy of Sciences of the United States of America 102, 16512–16517.Google Scholar
Romney, A.K., D’Andrade, R.G. & Indow, T. (2005). The distribution of response spectra in the lateral geniculate nucleus compared with reflectance spectra of Munsell color chips. Proceedings of the National Academy of Sciences of the United States of America 102, 9720–9725.Google Scholar
Roorda, A., Metha, A.B., Lennie, P. & Williams, D.R. (2001). Packing arrangement of the three cone classes in primate retina. Vision Research 41, 1291–1306.Google Scholar
Roy, S., Jayakumar, J., Martin, P.R., Dreher, B., Saalmann, Y.B., Hu, D. & Vidyasagar, T.R. (2009). Segregation of short-wavelength-sensitive (S) cone signals in the macaque dorsal lateral geniculate nucleus. Eur J Neurosci 30, 1517–1526.CrossRefGoogle ScholarPubMed
Salzman, C.D. & Newsome, W.T. (1994). Neural mechanisms for forming a perceptual decision. Science 264, 231–237.Google Scholar
Sciretta, P. (2009). Orange/Blue Contrast in Movie Posters. http://ohnotheydidnt.livejournal.com/41879586.html.Google Scholar
Seidemann, E., Poirson, A.B., Wandell, B.A. & Newsome, W.T. (1999). Color signals in area MT of the macaque monkey. Neuron 24, 911–917.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, 1123–1128.Google Scholar
Snodderly, D.M., Brown, P.K., Delori, F.C. & Auran, J.D. (1984). The macular pigment. I. Absorbance spectra, localization, and discrimination from other yellow pigments in primate retinas. Investigative Ophthalmology & Visual Science 25, 660–673.Google Scholar
Stockman, A. & Brainard, D.H. (2010). Color vision mechanisms. In The OSA Handbook of Optics (3rd ed.) ed. Bass, M., pp. 11.11–11.104. New York: McGraw-Hill.Google Scholar
Stoughton, C.M. & Conway, B.R. (2008). Neural basis for unique hues. Current Biology: CB 18, R698–R699.Google Scholar
Stoughton, C.M., Lafer-Sousa, R., Gagin, G. & Conway, B.R. (2012). Psychophysical chromatic mechanisms in macaque monkey. The Journal of Neuroscience 32, 15216–15226.Google Scholar
Sun, H., Smithson, H.E., Zaidi, Q. & Lee, B.B. (2006). Specificity of cone inputs to macaque retinal ganglion cells. Journal of Neurophysiology 95, 837–849.Google Scholar
Tanigawa, H., Lu, H.D. & Roe, A.W. (2010). Functional organization for color and orientation in macaque V4. Nature Neuroscience 13, 1542–1548.Google Scholar
Teufel, H.J. & Wehrhahn, C. (2004). Chromatic induction in humans: How are the cone signals combined to provide opponent processing? Vision Research 44, 2425–2435.Google Scholar
Thiele, A., Dobkins, K.R. & Albright, T.D. (2001). Neural correlates of chromatic motion perception. Neuron 32, 351–358.Google Scholar
Thorell, L.G., De Valois, R.L. & Albrecht, D.G. (1984). Spatial mapping of monkey V1 cells with pure color and luminance stimuli. Vision Research 24, 751–769.CrossRefGoogle ScholarPubMed
Tootell, R.B., Nelissen, K., Vanduffel, W. & Orban, G.A. (2004). Search for color ‘center(s)’ in macaque visual cortex. Cerebral Cortex 14, 353–363.Google Scholar
Vladusich, T. (2007). Chromatic aberration and the roles of double-opponent and color-luminance neurons in color vision. Neural Networks 20, 153–155.CrossRefGoogle ScholarPubMed
Wagner, G. & Boynton, R.M. (1972). Comparison of four methods of heterochromatic photometry. Journal of the Optical Society of America 62, 1508–1515.Google Scholar
Wandell, B.A., Poirson, A.B., Newsome, W.T., Baseler, H.A., Boynton, G.M., Huk, A., Gandhi, S. & Sharpe, L.T. (1999). Color signals in human motion-selective cortex. Neuron 24, 901–909.Google Scholar
Webster, M.A. (1996). Human colour perception and its adaptation. Network: Computation in Neural Systems 7, 587–634.Google Scholar
Webster, M.A., Miyahara, E., Malkoc, G. & Raker, V.E. (2000). Variations in normal color vision. II. Unique hues. Journal of the Optical Society of America. A, Optics, Image Science and Vision 17, 1545–1555.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.Google Scholar
Wray, J. & Edelman, G.M. (1996). A model of color vision based on cortical reentry. Cerebral Cortex 6, 701–716.Google Scholar
Xiao, Y., Casti, A., Xiao, J. & Kaplan, E. (2007). Hue maps in primate striate cortex. Neuroimage 35, 771–786.CrossRefGoogle ScholarPubMed
Xiao, Y., Wang, Y. & Felleman, D.J. (2003). A spatially organized representation of colour in macaque cortical area V2. Nature 421, 535–539.Google Scholar
Zeki, S. (1980). The representation of colours in the cerebral cortex. Nature 284, 412–418.Google Scholar
Zeki, S. (1983). The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex. Proceedings of the Royal Society of London. Series B, Biological Sciences 217, 449–470.Google Scholar
Zeki, S. (2004). Thirty years of a very special visual area, Area V5. The Journal of Physiology 557, 1–2.Google Scholar
Zeki, S.M. (1973). Colour coding in rhesus monkey prestriate cortex. Brain Research 53, 422–427.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1978). Functional specialisation in the visual cortex of the rhesus monkey. Nature 274, 423–428.Google Scholar