Color provides valuable information about the environment, yet the exact mechanisms explaining how colors appear to us remain poorly understood. Retinal signals are processed in the visual cortex through high-level mechanisms that link color perception with top-down expectations and knowledge. Here, we review the neuroimaging evidence about color processing in the brain, and how it is affected by acquired brain lesions in humans. Evidence from patients with brain-damage suggests that high-level color processing may be divided into at least three modules: perceptual color experience, color naming, and color knowledge. These modules appear to be functionally independent but richly interconnected, and serve as cortical relays linking sensory and semantic information, with the final goal of directing object-related behavior. We argue that the relations between colors and their objects are key mechanisms to understand high-level color processing.
AndrewsTJWatsonDMRiceGEHartleyT. 2015. Low-level properties of natural images predict topographic patterns of neural response in the ventral visual pathway. J Vis15(7):3. doi:10.1167/15.7.3
2.
BaizerJS. 1982. Receptive field properties of V3 neurons in monkey. Invest Ophthalmol Vis Sci23(1):87–95.
3.
BannertMMBartelsA. 2013. Decoding the yellow of a gray banana. Curr Biol23(22):2268–72. doi:10.1016/j.cub.2013.09.016
4.
BartolomeoP. 2002. The relationship between visual perception and visual mental imagery: a reappraisal of the neuropsychological evidence. Cortex38:357–78. doi:10.1016/S0010-9452(08)70665-8
5.
BartolomeoP. 2015. Visual imagery. In: WrightJDDella SalaS, eds. International encyclopedia of social and behavioral sciences. Amsterdam, Netherlands: Elsevier. p. 163–8.
6.
BartolomeoPBachoud-LéviACDe GelderBDenesG, DallaBarbaGBrugièresP, and others. 1998. Multiple-domain dissociation between impaired visual perception and preserved mental imagery in a patient with bilateral extrastriate lesions. Neuropsychologia36(3):239–49. doi:10.1016/s0028-3932(97)00103-6
7.
BartolomeoPBachoud-LéviACDenesG. 1997. Preserved imagery for colours in a patient with cerebral achromatopsia. Cortex33(2):369–78. doi:10.1016/S0010-9452(08)70012-1
8.
BartolomeoPBachoud-LéviACThiebautdeSchottenM. 2014. The anatomy of cerebral achromatopsia: a reappraisal and comparison of two case reports. Cortex56:138–44. doi:10.1016/j.cortex.2013.01.013
9.
BassoACapitaniELuzzattiCSpinnlerHZanobioME. 1985. Different basic components in the performance of Broca’s and Wernicke’s aphasics on the colour-figure matching test. Neuropsychologia23(1):51–9. doi:10.1016/0028-3932(85)90043-0
10.
BassoAFaglioniPSpinnlerH. 1976. Non-verbal colour impairment of aphasics. Neuropsychologia14(2):183–93. doi:10.1016/0028-3932(76)90047-6
11.
BeauvoisMFSaillantB. 1985. Optic aphasia for colours and colour agnosia: a distinction between visual and visuo-verbal impairments in the processing of colours. Cogn Neuropsychol2(1):1–48. doi:10.1080/02643298508252860
12.
BiedermanIJuG. 1988. Surface versus edge-based determinants of visual recognition. Cogn Psychol20(1):38–64. doi:10.1016/0010-0285(88)90024-2
13.
BohonKSHermannKLHansenTConwayBR. 2016. Representation of perceptual color space in macaque posterior inferior temporal cortex (the V4 complex). ENeuro3(4). doi:10.1523/ENEURO.0039-16.2016
14.
BornsteinMH. 1985. On the development of color naming in young children: data and theory. Brain Lang26(1):72–93. doi:10.1016/0093-934X(85)90029-X
15.
BouvierSEEngelSA. 2006. Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb Cortex16(2):183–91. doi:10.1093/cercor/bhi096
16.
BrewerAALiuJWadeARWandellBA. 2005. Visual field maps and stimulus selectivity in human ventral occipital cortex. Nat Neurosci8(8):1102–9. doi:10.1038/nn1507
17.
BrouwerGJHeegerDJ. 2009. Decoding and reconstructing color from responses in human visual cortex. J Neurosci29(44):13992–4003. doi:10.1523/JNEUROSCI.3577-09.2009
18.
BrouwerGJHeegerDJ. 2013. Categorical clustering of the neural representation of color. J Neurosci33(39):15454–65. doi:10.1523/JNEUROSCI.2472-13.2013
19.
BurkhalterAVan EssenDC. 1986. Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey. J Neurosci6(8):2327–51.
20.
CarotaACalabreseP. 2013. The achromatic “philosophical zombie”, a syndrome of cerebral achromatopsia with color anopsognosia. Case Rep Neurol5:98–103. doi:10.1159/000351027
21.
Cavina-PratesiCKentridgeRWHeywoodCAMilnerAD. 2010. Separate channels for processing form, texture, and color: evidence from fMRI adaptation and visual object agnosia. Cereb Cortex20:2319–32. doi:10.1093/cercor/bhp298
22.
ChaoLLMartinA. 1999. Cortical regions associated with perceiving, naming, and knowing about colors. J Cogn Neurosci11(1):25–35.
23.
ChicaABBartolomeoP. 2012. Attentional routes to conscious perception. Front Psychol3, 1. doi:10.3389/fpsyg.2012.00001
24.
ConwayBR. 2001. Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1). J Neurosci21(8):2768–83. doi:10.1523/JNEUROSCI.21-08-02768.2001
25.
ConwayBR. 2009. Color vision, cones, and color-coding in the cortex. Neuroscientist15(3):274–90. doi:10.1177/1073858408331369
26.
ConwayBR. 2014. Color signals through dorsal and ventral visual pathways. Vis Neurosci31(2):197–209. doi:10.1017/S0952523813000382.Color
27.
ConwayBR. 2018. The organization and operation of inferior temporal cortex. Annu Rev Vis Sci4:381–420. doi:10.1146/annurev-vision-091517-034202
28.
ConwayBRChatterjeeSFieldGDHorwitzGDJohnsonENKoidaK, and others. 2010. Advances in color science: from retina to behavior. J Neurosci30(45):14955–63. doi:10.1523/JNEUROSCI.4348-10.2010
29.
ConwayBRMoellerSTsaoDY. 2007. Specialized color modules in macaque extrastriate cortex. Neuron56(3):560–73. doi:10.1016/j.neuron.2007.10.008
30.
CuthillICAllenWLArbuckleKCaspersBChaplinGHauberME, and others. 2017. The biology of color. Science357(6350):eaan0221. doi:10.1126/science.aan0221
31.
DamasioADamasioH. 1983. The anatomic basis of pure alexia. Neurology33(12):1573–83. doi:10.1212/WNL.33.12.1573
32.
DavidoffJ. 1996. Lewandowsky’s case of object-colour agnosia. In: CodeCWalleschCWJoanetteYLecoursAR, eds. Classic cases in neuropsychology. Hove, East Sussex: Psychology Press. p. 133–44.
33.
DavidoffJFodorG. 1989. An annotated translation of Lewandowsky (1908). Cogn Neuropsychol6(2):165–77. doi:10.1080/02643298908253417
34.
DavidoffJOstergaardAL. 1984. Colour anomia resulting from weakened short-term colour memory: a case study. Brain107(2):415–31. doi:10.1093/brain/107.2.415
35.
De RenziESpinnlerH. 1967. Impaired performance on color tasks in patients with hemispheric damage. Cortex3(2):194–217. doi:10.1016/S0010-9452(67)80012-1
36.
De ValoisRLAbramovIJacobsGH. 1966. Analysis of response patterns of LGN cells. J Opt Soc Am56(7):966–77.
37.
De VreeseLP. 1988. Category-specific versus modality-specific aphasia for colours: a review of the pioneer case studies. Int J Neurosci43(3–4):195–206. doi:10.3109/00207458808986170
38.
De VreeseLP. 1991. Two systems for colour-naming defects: Verbal disconnection vs colour imagery disorder. Neuropsychologia29(1):1–18. doi:10.1016/0028-3932(91)90090-U
39.
DehaeneSChangeuxJP. 2011. Experimental and theoretical approaches to conscious processing. Neuron70(2):200–27. doi:10.1016/j.neuron.2011.03.018
40.
DehaeneSNaccacheL. 2001. Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition79(1–2):1–37. doi:10.1016/S0010-0277(00)00123-2
41.
DerringtonAMKrauskopfJLennieP. 1984. Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol357:241–65.
42.
EskewRT. 2009. Higher order color mechanisms: a critical review. Vis Res49(22):2686–704. doi:10.1016/j.visres.2009.07.005
43.
FineIMacLeodDBoyntonGM. 2003. Surface segmentation based on the luminance and color statistics of natural scenes. J Vis20(7):1283–91. doi:10.1167/2.10.66
44.
FreiwaldWATsaoDY. 2010. Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science330(6005):845–51. doi:10.1126/science.1194908
45.
FukuzawaKItohMSasanumaSSuzukiTFukusakoYMasuiT. 1988. Internal representations and the conceptual operation of color in pure alexia with color naming defects. Brain Lang34(1):98–126. doi:10.1016/0093-934X(88)90126-5
GegenfurtnerKRKiperDC. 2003. Color vision. Annu Rev Neurosci26(1):181–206. doi:10.1146/annurev.neuro.26.041002.131116
48.
GegenfurtnerKRKiperDCLevittJB. 1997. Functional properties of neurons in macaque area V3. J Neurophysiol77(4):1906–23. doi:10.1152/jn.1997.77.4.1906
49.
GeschwindNFusilloM. 1966. Color-naming defects in association with alexia. Arch Neurol15:137–46. doi:10.1001/archneur.1966.00470140027004
50.
Grill-SpectorKWeinerKS. 2014. The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci15(8):536–48. doi:10.1038/nrn3747
51.
HansenTGegenfurtnerKR. 2009. Independence of color and luminance edges in natural scenes. Vis Neurosci26(1):35–49. doi:10.1017/s0952523808080796
52.
HansenTOlkkonenMWalterSGegenfurtnerKR. 2006. Memory modulates color appearance. Nat Neurosci9(11):1367–8. doi:10.1038/nn1794
53.
HeywoodCAKentridgeRW. 2003. Achromatopsia, color vision, and cortex. Neurol Clin21(2):483–500.
54.
HorwitzGDHassCA. 2012. Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing. Nat Neurosci15(6):913–9. doi:10.1038/nn.3105
55.
KentridgeRWHeywoodCACoweyA. 2004. Chromatic edges, surfaces and constancies in cerebral achromatopsia. Neuropsychologia42(6):821–30. doi:10.1016/j.neuropsychologia.2003.11.002
56.
KentridgeRWHeywoodCAWeiskrantzL. 2007. Color contrast processing in human striate cortex. Proc Natl Acad Sci U S A104(38):15129–31. doi:10.1073/pnas.0706603104
57.
KingdomFABeauceCHunterL. 2004. Colour vision brings clarity to shadows. Perception33(8):907–14. doi:10.1068/p5264
KiperDCFenstemakerSBGegenfurtnerKR. 1997. Chromatic properties of neurons in macaque area V2. Vis Neurosci14(6):1061–72.
60.
KosslynSMThompsonWLGanisG. 2010. The case for mental imagery. The Case for Mental Imagery. doi:10.1093/acprof:oso/9780195179088.001.0001
61.
KowalskiKZimilesH. 2006. The relation between children’s conceptual functioning with color and color term acquisition. J Exp Child Psychol94(4):301–21. doi:10.1016/j.jecp.2005.12.001
62.
KrauskopfJWilliamsDRHeeleyDW. 1982. Cardinal directions of color space. Vis Res22(9):1123–31.
63.
Lafer-SousaRConwayBR. 2013. Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat Neurosci16(12):1870–8. doi:10.1038/nn.3555
64.
Lafer-SousaRConwayBRKanwisherNG. 2016. Color-biased regions of the ventral visual pathway lie between face- and place-selective regions in humans, as in macaques. J Neurosci36(5):1682–97. doi:10.1523/JNEUROSCI.3164-15.2016
65.
Lafer-SousaRHermannKLConwayBR. 2015. Striking individual differences in color perception uncovered by “the dress” photograph. Curr Biol25(13):R545–R546. doi:10.1016/J.CUB.2015.04.053
66.
Lafer-SousaRLiuYOLafer-SousaLWiestMCConwayBR. 2012. Color tuning in alert macaque V1 assessed with fMRI and single-unit recording shows a bias toward daylight colors. J Opt Soc Am29(5):657–70. doi:10.1364/JOSAA.29.000657
67.
LimHWangYXiaoYHuMFellemanDJ. 2009. Organization of hue selectivity in macaque V2 thin stripes. J Neurophysiol102(5):2603–15. doi:10.1152/jn.91255.2008
68.
LuzzattiCDavidoffJ. 1994. Impaired retrieval of object-colour knowledge with perserved colour naming. Neuropsychologia32(8):933–50.
69.
McKeefryDZekiS. 1997. The position and topography of the human colour centre as revealed by functional magnetic resonance imaging. Brain120(12):2229–42. doi:10.1093/brain/120.12.2229
70.
MiceliGFouchECapassoRSheltonJRTomaiuoloFCaramazzaA. 2001. The dissociation of color from form and function knowledge. Nat Neurosci4(6):662–7. doi:10.1038/88497
71.
MohrJPLeicesterJStoddardLTSidmanM. 1971. Right hemianopia with memory and color deficits in circumscribed left posterior cerebral artery territory infarction. Neurology21:1104–13. doi:10.1212/wnl.21.11.1104
72.
MollonJD. 1989. “Tho’ she kneel’d in that place where they grew . . .” The uses and origins of primate colour vision. J Exp Biol146(1):21–38.
73.
MoutoussisKZekiS. 2002. Responses of spectrally selective cells in macaque area V2 to wavelengths and colors. J Neurophysiol87(4):2104–12. doi:10.1152/jn.00248.2001
74.
MullenKTChangDHHessRF. 2015. The selectivity of responses to red-green colour and achromatic contrast in the human visual cortex: an fMRI adaptation study. Eur J Neurosci42(11):2923–33. doi:10.1111/ejn.13090
75.
MullenKTDumoulinSOMcMahonKLDe ZubicarayGIHessRF. 2007. Selectivity of human retinotopic visual cortex to S-cone-opponent, L/M-cone-opponent and achromatic stimulation. Eur J Neurosci25(2):491–502. doi:10.1111/j.1460-9568.2007.05302.x
76.
MurpheyDKYoshorDBeauchampMS. 2008. Perception matches selectivity in the human anterior color center. Curr Biol18(3):216–20. doi:10.1016/j.cub.2008.01.013
77.
OxburyJMOxburySMHumphreyNK. 1969. Varieties of colour anomia. Brain92(4):847–60. doi:10.1093/brain/92.4.847
78.
PárragaCATrosciankoTTolhurstDJ. 2002. Spatiochromatic properties of natural images and human vision. Curr Biol12(6):483–7.
79.
PersichettiASThompson-SchillSLButtOHBrainardDHAguirreGK. 2015. Functional magnetic resonance imaging adaptation reveals a noncategorical representation of hue in early visual cortex. J Vis15(6):18. doi:10.1167/15.6.18
80.
PriceCJMooreCJHumphreysGWFrackowiakRSFristonKJ. 1996. The neural regions sustaining object recognition and naming. Proc R Soc B Biol Sci263(1376):1501–7. doi:10.1098/rspb.1996.0219
81.
RiddochMJHumphreysGWGannonTBlottWJonesV. 1999. Memories are made of this: the effects of time on stored visual knowledge in a case of visual agnosia. Brain122(3):537–59. doi:10.1093/brain/122.3.537
82.
RiesenhuberMPoggioT. 1999. Hierarchical models of object recognition in cortex. Nat Neurosci2(11):1019–25. doi:10.1038/14819
83.
RosenthalIRatnasingamSHaileTEastmanSFuller-DeetsJConwayBR. 2018. Color statistics of objects, and color tuning of object cortex in macaque monkey. J Vis18(11):1. doi:10.1167/18.11.1
84.
SchalkGKapellerCGugerCOgawaHHiroshimaSLafer-SousaR, and others. 2017. Facephenes and rainbows: causal evidence for functional and anatomical specificity of face and color processing in the human brain. Proc Natl Acad Sci U S A114(46):12285–90. doi:10.1073/pnas.1713447114
85.
SetäläKVestiE. 1994. Acquired cerebral achromatopsia: a case report. Neuro-Ophthalmology14(1):31–6. doi:10.3109/01658109409019483
86.
ShapleyRHawkenMJ. 2011. Color in the cortex: single- and double-opponent cells. Vis Res51:701–17. doi:10.1016/j.visres.2011.02.012
87.
ShepardTGLahlafSIEskewRT. 2017. Labeling the lines: a test of a six-mechanism model of chromatic detection. J Vis17(13):9. doi:10.1167/17.13.9
88.
ShortRAGraff-RadfordNR. 2001. Localization of hemiachromatopsia. Neurocase7(4):331–7. doi:10.1093/neucas/7.4.331
89.
SimmonsWKRamjeeVBeauchampMSMcRaeKMartinABarsalouLW. 2007. A common neural substrate for perceiving and knowing about color. Neuropsychologia45(12):2802–10. doi:10.1016/j.neuropsychologia.2007.05.002.A
90.
Siuda-KrzywickaKBorosMBartolomeoPWitzelC. 2019a. The biological bases of colour categories: from goldfish to the human brain. Cortex118:82–106. doi:10.1016/j.cortex.2019.04.010
91.
Siuda-KrzywickaKWitzelCChabaniETagaMCosteCCoolsN, and others. 2019b. Color categorisation independent of color naming. Cell Rep28:2471–9. doi:10.1016/j.celrep.2019.08.003
92.
Siuda-KrzywickaKWitzelCTagaMDelanoeMCohenLBartolomeoP. 2019c. When colours split from objects: the disconnection of colour perception from colour language and colour knowledge. Cogn Neuropsychol. Epub Sep3. doi:10.1080/02643294.2019.1642861
93.
SojaNN. 1994. Young children’s concept of color and its relation to the acquisition of color words. Child Dev65(3):918. doi:10.2307/1131428
94.
StachowiakFJPoeckK. 1976. Functional disconnection in pure alexia and color naming deficit demonstrated by facilitation methods. Brain Lang3(1):135–43. doi:10.1016/0093-934X(76)90010-9
95.
StasenkoAGarceaFEDombovyMMahonBZ. 2014. When concepts lose their color: a case of object-color knowledge impairment. Cortex58:217–38. doi:10.1016/j.cortex.2014.05.013
96.
StengelEViennaMDEdinL. 1947. The syndrome of visual alexia with colour agnosia. The British Journal of Psychiatry94(394): 46–58. doi:10.1192/bjp.94.394.46
97.
TanakaJWeiskopfDWilliamsP. 2001. The role of color in high-level vision. Trends Cogn Sci5(5):211–5. doi:10.1016/S1364-6613(00)01626-0
98.
Van ZandvoortMJNijboerTCde HaanE. 2007. Developmental colour agnosia. Cortex43:750–7.
99.
VandenbrouckeREFahrenfortJJMeuweseJDScholteHSLammeV. 2014. Prior knowledge about objects determines neural color representation in human visual cortex. Cereb Cortex26(4):1401–8. doi:10.1093/cercor/bhu224
100.
VerreyD. 1888. Hemiachromatopsie droite absolue. Conservation partielle de la perception lumineuse et des formes. Ancien kyste hemorhagique de la partie inferieur due lobe occipital gauche. Arch Opthalmol (Paris) (Vol. 8).
101.
WadeARBrewerAARiegerJWWandellBA. 2002. Functional measurements of human ventral occipital cortex: retinotopy and colour. Philos Trans R Soc B Biol Sci357(1424):963–73. doi:10.1098/rstb.2002.1108
102.
WangLREBMruczekArcaroMJKastnerS.2015. Probabilistic maps of visual topography in human cortex. Cerebral Cortex25(10): 3911–31. doi:10.1093/cercor/bhu277
103.
WilbrandH. 1887. Die Seelenblindheit als Herderscheinung. Weisbaden, Germany: Bergmann.
104.
WitzelCGegenfurtnerKR. 2018. Color perception: objects, constancy, and categories. Annu Rev Vis Sci4(1):16.1-16.25. doi:10.1146/annurev-vision-091517-034231
105.
WitzelCRaceyCO’ReganJK. 2017. The most reasonable explanation of “the dress”: implicit assumptions about illumination. J Vis17(2):1. doi:10.1167/17.2.1
WoodwardTSDixonMJMullenKTChristensenKMBubDN. 1999. Analysis of errors in color agnosia: a single-case study. Neurocase5(2):95–108. doi:10.1093/neucas/5.2.95
108.
XiaoYWangYFellemanDJ. 2003. A spatially organized representation of colour in macaque cortical area V2. Nature421(6922):535–9. doi:10.1038/nature01372
109.
YoonessiAKingdomFAAlqawlaqS. 2008. Is color patchy?J Opt Soc Am25(6):1330–8.
110.
ZekiSMariniL. 1998. Three cortical stages of colour processing in the human brain. Brain121(9):1669–85. doi:10.1093/brain/121.9.1669
