Color in the Cortex

We begin with a discussion of the role of human color vision, asking what value the possession of color vision adds to the perception of the natural scene, both in terms of our ability to see color differences (contrast) and in color identification. We then consider the psychophysical properties of cortical color vision and what they reveal about its use in determining shape and form. We pit against each other different models accounting for how achromatic (luminance) contrast and color contrast may be linked in the determination of shape, comparing a coloring book model, in which color plays only a subordinate or minor role, an intrinsic images model in which color contrast makes an independent contribution, and an integration model in which color and luminance contrast both provide cue-invariant form information to color–luminance shape detectors. These models are also interpreted in the light of what we know about the physiological basis of color vision through primate single cell recordings, particularly in area V1. Finally, we discuss what has been revealed about human color vision in V1 and extra striate cortex from fMRI studies.

[1]  Jonathan E. Jennings,et al.  An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. , 1999, Cerebral cortex.

[2]  R. L. Valois Analysis and coding of color vision in the primate visual system. , 1965 .

[3]  K. Mullen,et al.  The role of perception, language, and preference in the developmental acquisition of basic color terms. , 2005, Journal of experimental child psychology.

[4]  H. Komatsu,et al.  Neural selectivity for hue and saturation of colour in the primary visual cortex of the monkey , 2000, The European journal of neuroscience.

[5]  C. P. Biggam The Semantics of Colour: Basic colour terms , 2012 .

[6]  Bevil R. Conway,et al.  Spatial Structure of Cone Inputs to Color Cells in Alert Macaque Primary Visual Cortex (V-1) , 2001, The Journal of Neuroscience.

[7]  Tobias E. Reisbeck,et al.  PII: S0042-6989(97)00240-X , 2003 .

[8]  H. Barrow,et al.  RECOVERING INTRINSIC SCENE CHARACTERISTICS FROM IMAGES , 1978 .

[9]  D. H. Kelly Spatiotemporal variation of chromatic and achromatic contrast thresholds. , 1983, Journal of the Optical Society of America.

[10]  Anitha Pasupathy,et al.  Equiluminance Cells in Visual Cortical Area V4 , 2011, The Journal of Neuroscience.

[11]  C. Stromeyer,et al.  Visual interactions with luminance and chromatic stimuli. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[12]  D. G. Albrecht,et al.  Spatial mapping of monkey VI cells with pure color and luminance stimuli , 1984, Vision Research.

[13]  K. Mullen,et al.  The spatial tuning of chromatic mechanisms identified by simultaneous masking , 1994, Vision Research.

[14]  Jens Frahm,et al.  Functional mapping of color processing by magnetic resonance imaging of responses to selective P- and M-pathway stimulation , 1996, Experimental Brain Research.

[15]  N. Daw,et al.  Goldfish Retina: Organization for Simultaneous Color Contrast , 1967, Science.

[16]  Bevil R. Conway,et al.  Spatial and Temporal Properties of Cone Signals in Alert Macaque Primary Visual Cortex , 2006, The Journal of Neuroscience.

[17]  R. Eskew Chromatic Detection and Discrimination , 2008 .

[18]  Karl R Gegenfurtner,et al.  Geometry in Nature , 1993 .

[19]  A. Leventhal,et al.  Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[21]  K T Mullen,et al.  Bipolar or rectified chromatic detection mechanisms? , 2001, Visual Neuroscience.

[22]  K. Koffka Principles Of Gestalt Psychology , 1936 .

[23]  Frederick A A Kingdom,et al.  Colour Vision Brings Clarity to Shadows , 2004, Perception.

[24]  J. Nathans,et al.  Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. , 1986, Science.

[25]  K. Mullen,et al.  Postreceptoral chromatic detection mechanisms revealed by noise masking in three-dimensional cone contrast space. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[26]  H. B. Barlow,et al.  What does the eye see best? , 1983, Nature.

[27]  S. Zeki Colour coding in the cerebral cortex: The responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition , 1983, Neuroscience.

[28]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[29]  J. Mollon "Tho' she kneel'd in that place where they grew..." The uses and origins of primate colour vision. , 1989, The Journal of experimental biology.

[30]  DH Hubel,et al.  Psychophysical evidence for separate channels for the perception of form, color, movement, and depth , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  D. Tolhurst,et al.  Spatiochromatic Properties of Natural Images and Human Vision , 2002, Current Biology.

[32]  E. Seidemann,et al.  Color Signals in Area MT of the Macaque Monkey , 1999, Neuron.

[33]  R. Shapley,et al.  The spatial transformation of color in the primary visual cortex of the macaque monkey , 2001, Nature Neuroscience.

[34]  Barry B. Lee,et al.  Temporal frequency and chromatic processing in humans: an fMRI study of the cortical visual areas. , 2011, Journal of vision.

[35]  C. F. Stromeyer,et al.  Colour is what the eye sees best , 1993, Nature.

[36]  G. Horwitz,et al.  Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing , 2012, Nature Neuroscience.

[37]  G. H. Jacobs Primate color vision: A comparative perspective , 2008, Visual Neuroscience.

[38]  Daniel C Kiper,et al.  The detection of colored Glass patterns. , 2003, Journal of vision.

[39]  B. Wandell,et al.  Specializations for Chromatic and Temporal Signals in Human Visual Cortex , 2005, Journal of Neuroscience.

[40]  T. Sejnowski,et al.  Representation of Color Stimuli in Awake Macaque Primary Visual Cortex , 2003, Neuron.

[41]  J. Nathans The Evolution and Physiology of Human Color Vision Insights from Molecular Genetic Studies of Visual Pigments , 1999, Neuron.

[42]  Kathy T. Mullen,et al.  Orientation tuning in human colour vision at detection threshold , 2014, Scientific Reports.

[43]  Alex R. Wade,et al.  Visual field maps and stimulus selectivity in human ventral occipital cortex , 2005, Nature Neuroscience.

[44]  C. Gross,et al.  Color categories in macaques. , 1979, Journal of comparative and physiological psychology.

[45]  E Switkes,et al.  Simultaneous masking interactions between chromatic and luminance gratings. , 1983, Journal of the Optical Society of America.

[46]  Gregory D Horwitz,et al.  V1 mechanisms underlying chromatic contrast detection. , 2013, Journal of neurophysiology.

[47]  H. Komatsu,et al.  Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex , 2007, Nature Neuroscience.

[48]  J. Y. Goulermas,et al.  Multivoxel fMRI analysis of color tuning in human primary visual cortex. , 2009, Journal of vision.

[49]  S. Engel,et al.  Color opponent neurons in V1: a review and model reconciling results from imaging and single-unit recording. , 2002, Journal of vision.

[50]  R. Hess,et al.  Responses of the human visual cortex and LGN to achromatic and chromatic temporal modulations: an fMRI study. , 2010, Journal of vision.

[51]  A. James,et al.  Retinotopic distribution of chromatic responses in human primary visual cortex , 2006, The European journal of neuroscience.

[52]  P. Dean,et al.  Visual cortex ablation and thresholds for successively presented stimuli in rhesus monkeys: II. Hue , 1979, Experimental Brain Research.

[53]  Robert Shapley,et al.  Brightness–Color Interactions in Human Early Visual Cortex , 2015, The Journal of Neuroscience.

[54]  Jules Davidoff,et al.  Impaired retrieval of object-colour knowledge with preserved colour naming , 1994, Neuropsychologia.

[55]  Arthur Bradley,et al.  Orientation and spatial frequency selectivity of adaptation to color and luminance gratings , 1988, Vision Research.

[56]  Sophie M. Wuerger,et al.  Input of long- and middle-wavelength-sensitive cones to orientation discrimination , 1999 .

[57]  J. Mollon,et al.  Dichromats detect colour-camouflaged objects that are not detected by trichromats , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  Kathy T Mullen,et al.  Contour integration in color vision: a common process for the blue–yellow, red–green and luminance mechanisms? , 2000, Vision Research.

[59]  K T Mullen,et al.  Evidence for separate pathways for color and luminance detection mechanisms. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[60]  R. M. Boynton,et al.  Categorical color perception of Japanese observers: Comparison with that of Americans , 1987, Vision Research.

[61]  Bevil R. Conway,et al.  Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex , 2013, Nature Neuroscience.

[62]  R. Shapley,et al.  Cone inputs in macaque primary visual cortex. , 2004, Journal of Neurophysiology.

[63]  Marc H. Bornstein,et al.  On the development of color naming in young children: Data and theory , 1985, Brain and Language.

[64]  R. Shapley,et al.  Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus , 1992, Nature.

[65]  K. Mullen The contrast sensitivity of human colour vision to red‐green and blue‐yellow chromatic gratings. , 1985, The Journal of physiology.

[66]  J. Mollon,et al.  Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[67]  C. Furmanski,et al.  Selective Adaptation to Color Contrast in Human Primary Visual Cortex , 2001, The Journal of Neuroscience.

[68]  C. F. Stromeyer,et al.  Separable red-green and luminance detectors for small flashes , 1994, Vision Research.

[69]  Michael S. Gazzaniga,et al.  Acquired central dyschromatopsia: Analysis of a case with preservation of color discrimination , 1989 .

[70]  P. Lennie,et al.  Chromatic Gain Controls in Visual Cortical Neurons , 2005, The Journal of Neuroscience.

[71]  K. Mullen,et al.  Analysis of errors in color agnosia: A single-case study , 1999 .

[72]  D. Teller Spatial and temporal aspects of infant color vision , 1998, Vision Research.

[73]  D. Burr,et al.  Development of infant contrast sensitivity to chromatic stimuli , 1993, Vision Research.

[74]  R. Shapley,et al.  Color in the Cortex: single- and double-opponent cells , 2011, Vision Research.

[75]  Rhea T Eskew,et al.  Chromatic masking in the (ΔL/L, ΔM/M) plane of cone-contrast space reveals only two detection mechanisms , 1998, Vision Research.

[76]  A. Mizuno,et al.  A change of the leading player in flow Visualization technique , 2006, J. Vis..

[77]  R. Shapley,et al.  The Orientation Selectivity of Color-Responsive Neurons in Macaque V1 , 2008, The Journal of Neuroscience.

[78]  J. Davidoff,et al.  Colour categories in a stone-age tribe , 1999, Nature.

[79]  S. Shevell,et al.  Color in complex scenes. , 2008, Annual review of psychology.

[80]  P. Cavanagh,et al.  Retinotopy and color sensitivity in human visual cortical area V8 , 1998, Nature Neuroscience.

[81]  Kai-Fu Yang,et al.  Color Constancy Using Double-Opponency , 2015, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[82]  Fang Liu,et al.  Perceptual Color Map in Macaque Visual Area V4 , 2014, The Journal of Neuroscience.

[83]  S. Zeki,et al.  The position and topography of the human colour centre as revealed by functional magnetic resonance imaging. , 1997, Brain : a journal of neurology.

[84]  H. Spekreijse,et al.  The “silent substitution” method in visual research , 1982, Vision Research.

[85]  Daniel C. Kiper,et al.  Distributed processing of color and form in the visual cortex , 2013, Front. Psychol..

[86]  D. Brainard,et al.  Aberration-free measurements of the visibility of isoluminant gratings. , 1993, Journal of the Optical Society of America. A, Optics, image science, and vision.

[87]  V. Walsh,et al.  Higher-level cortical processing of colour. , 1997, Acta psychologica.

[88]  H B Barlow,et al.  The Ferrier lecture, 1980 , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[89]  H. Barlow Critical limiting factors in the design of the eye and visual cortex , 1981 .

[90]  K. Mullen,et al.  Contrast normalization in colour vision: the effect of luminance contrast on colour contrast detection , 2014, Scientific Reports.

[91]  Kathy T Mullen,et al.  Comparison of color and luminance vision on a global shape discrimination task , 2002, Vision Research.

[92]  S Yamane,et al.  Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  C. F. Stromeyer,et al.  Second-site adaptation in the red-green chromatic pathways , 1985, Vision Research.

[94]  C F Stromeyer,et al.  Detection uncertainty and the facilitation of chromatic detection by luminance contours. , 1991, Journal of the Optical Society of America. A, Optics and image science.

[95]  S. Deeb,et al.  Genetics of variation in human color vision and the retinal cone mosaic. , 2006, Current opinion in genetics & development.

[96]  A Bradley,et al.  Contrast dependence and mechanisms of masking interactions among chromatic and luminance gratings. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[97]  Algis J. Vingrys,et al.  Visual thresholds measured with color video monitors , 1987 .

[98]  R. Hess,et al.  Selectivity of human retinotopic visual cortex to S‐cone‐opponent, L/M‐cone‐opponent and achromatic stimulation , 2007, The European journal of neuroscience.

[99]  Mullen,et al.  PII: S0042-6989(98)00171-0 , 1998 .

[100]  P. Lennie,et al.  Chromatic mechanisms in striate cortex of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[101]  M. Vorobyev Ecology and evolution of primate colour vision , 2004, Clinical & experimental optometry.

[102]  Darren Van Laar,et al.  The structure of colour naming space , 2000, Vision Research.

[103]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. V. Multivariate statistical analyses and models. , 1976, Journal of neurophysiology.

[104]  A Bradley,et al.  Failures of isoluminance caused by ocular chromatic aberrations. , 1992, Applied optics.

[105]  J. Mollon,et al.  Fruits, foliage and the evolution of primate colour vision. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[106]  A. Bartels,et al.  Decoding the Yellow of a Gray Banana , 2013, Current Biology.

[107]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[108]  Hong Zhou,et al.  The coding of uniform colour figures in monkey visual cortex , 2003, The Journal of physiology.

[109]  M. Bornstein,et al.  Perceptual categorization of color: A life-span study , 1983, Psychological research.

[110]  K R Gegenfurtner,et al.  Contrast detection in luminance and chromatic noise. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[111]  Yongjie Li,et al.  A Color Constancy Model with Double-Opponency Mechanisms , 2013, 2013 IEEE International Conference on Computer Vision.

[112]  R. Vimal,et al.  ORIENTATION TUNING OF THE SPATIAL-FREQUENCY-TUNED MECHANISMS OF THE RED-GREEN CHANNEL , 1997 .

[113]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[114]  S. Zeki,et al.  Has a new color area been discovered? , 1998, Nature Neuroscience.

[115]  R. Hess,et al.  Response of the human LGN to different temporal frequencies for achromatic, L/M opponent and S-cone opponent stimuli measured with high field fMRI , 2010 .

[116]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[117]  Stephen A Engel,et al.  Adaptation of Oriented and Unoriented Color-Selective Neurons in Human Visual Areas , 2005, Neuron.

[118]  Hugh R. Wilson,et al.  Spatial-frequency adaptation: Evidence for a multiple-channel model of short-wavelength-sensitive-cone spatial vision , 1993, Vision Research.

[119]  Frederick A A Kingdom,et al.  Color brings relief to human vision , 2003, Nature Neuroscience.

[120]  K. Mullen,et al.  Is the Acquisition of Basic-Colour Terms in Young Children Constrained? , 2002, Perception.

[121]  Dorita H. F. Chang,et al.  The selectivity of responses to red‐green colour and achromatic contrast in the human visual cortex: an fMRI adaptation study , 2015, The European journal of neuroscience.

[122]  K. Mullen,et al.  Estimation of the L-, M-, and S-cone weights of the postreceptoral detection mechanisms , 1996 .

[123]  Kathy T Mullen,et al.  Blobs versus bars: psychophysical evidence supports two types of orientation response in human color vision. , 2013, Journal of vision.

[124]  Gouki Okazawa,et al.  Effects of Luminance Contrast on the Color Selectivity of Neurons in the Macaque Area V4 and Inferior Temporal Cortex , 2014, The Journal of Neuroscience.

[125]  K. Mullen,et al.  Absence of Linear Subthreshold summation between Red-Green and Luminance Mechanisms over a Wide Range of Spatio-temporal Conditions , 1997, Vision Research.

[126]  Bevil R. Conway,et al.  Specialized Color Modules in Macaque Extrastriate Cortex , 2007, Neuron.

[127]  Kathy T. Mullen,et al.  Contour integration with colour and luminance contrast , 1996, Vision Research.

[128]  K. Mullen,et al.  Evidence for the stochastic independence of the blue-yellow, red-green and luminance detection mechanisms revealed by subthreshold summation , 1999, Vision Research.

[129]  J. Mollon Monge: The Verriest Lecture, Lyon, July 2005 , 2006, Visual Neuroscience.

[130]  K. Mullen,et al.  Orientation selectivity in luminance and color vision assessed using 2-d band-pass filtered spatial noise , 2005, Vision Research.

[131]  H. Wilson,et al.  Spatial frequency mechanisms with short-wavelength-sensitive cone inputs , 1992, Vision Research.

[132]  L. Sharpe,et al.  Hue memory and discrimination in young children , 1998, Vision Research.

[133]  K. Wolf Visual Ecology: Coloured Fruit is What the Eye Sees Best , 2002, Current Biology.

[134]  Guillermo Sapiro,et al.  A subspace reverse-correlation technique for the study of visual neurons , 1997, Vision Research.

[135]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[136]  Kai-Fu Yang,et al.  Boundary Detection Using Double-Opponency and Spatial Sparseness Constraint , 2015, IEEE Transactions on Image Processing.

[137]  Alex R. Wade,et al.  fMRI measurements of color in macaque and human. , 2008, Journal of vision.

[138]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[139]  H. A. Pham,et al.  Perceptual deficits after lesions of inferotemporal cortex in macaques. , 2000, Cerebral cortex.

[140]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[141]  W. McIlhagga,et al.  Detection mechanisms in L-, M-, and S-cone contrast space. , 1993, Journal of the Optical Society of America. A, Optics and image science.

[142]  Colin W G Clifford,et al.  Interactions between color and luminance in the perception of orientation. , 2003, Journal of vision.

[143]  K. D. De Valois,et al.  Orientation and spatial-frequency discrimination for luminance and chromatic gratings. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[144]  R. Shapley,et al.  Space and Time Maps of Cone Photoreceptor Signals in Macaque Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[145]  Brian A Wandell,et al.  Visual field map clusters in human cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[146]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[147]  Anthony M. Norcia,et al.  Does chromatic sensitivity develop more slowly than luminance sensitivity? , 1993, Vision Research.

[148]  T. Albright,et al.  Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1. , 2005, Journal of neurophysiology.

[149]  Bevil R. Conway,et al.  Color contrast in macaque V1. , 2002, Cerebral cortex.

[150]  Marie-Juliette F Mandelli,et al.  The local and global processing of chromatic Glass patterns. , 2005, Journal of vision.

[151]  K. Mullen,et al.  Color and luminance spatial tuning estimated by noise masking in the absence of off-frequency looking. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

[152]  K. Mullen,et al.  Evidence that global processing does not limit thresholds for RF shape discrimination. , 2011, Journal of vision.

[153]  S. Zeki Colour coding in the cerebral cortex: The reaction of cells in monkey visual cortex to wavelengths and colours , 1983, Neuroscience.

[154]  Karl J. Friston,et al.  The colour centre in the cerebral cortex of man , 1989, Nature.