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Human Trichromacy Revisited PNAS PLUS Human trichromacy revisited PNAS PLUS Hiroshi Horiguchia,b,1, Jonathan Winawera, Robert F. Doughertyc, and Brian A. Wandella,c aPsychology Department, Stanford University, Stanford, CA 94305; bDepartment of Ophthalmology, School of Medicine, Jikei University, Tokyo 105-8461, Japan; and cStanford Center for Cognitive and Neurobiological Imaging, Stanford, CA 94305 AUTHOR SUMMARY The history of trichromatic color As predicted by the classic tri- theory spans nearly 300 y, be- msARC Fovea Periphery chromatic model, subjects fail to ’ Opticks (%) ginning with Newton s 10 see cone-silent stimuli presented (1). Thomas Young’s Royal So- Visible in the fovea. In contrast, subjects Not ciety Lecture (2) explained how 0 Not do see cone-silent stimuli pre- Visible Visible Visible Visible color perception is initiated by S1 sented to the peripheral visual S2 fi the absorption of light in three Cone-silent −10 eld. In extensive computational S3 fi types of human light receptors, −10 0 10 −10 0 10 (%) modeling, we could nd no plau- the cones. The theory of tri- S-cone S-cone sible pigment density adjustment chromacy is the foundation of (including the lens or photopig- modern color technologies (3). Fig. P1. Built and found. (A) An apparatus using six primary lights was ment densities) that explains the built for the experiment. Mean luminance through the eyepiece was measurements in the periphery For more than a century, the 2 absorption of light in the retina 2,060 cd/m .(B) Graphs represent detection thresholds for stimuli that based on a model that includes was thought to occur only in the have some S-cone contrast and cone-silent contrast, but no L- or M- only three cone photopigments. cone contrast. In foveal presentation, both subjects S1 and S2 detected photoreceptor layer: in the rods Rather, the data support a model 10% S-cone modulation. Cone-silent contrast was invisible to both — in low light (scotopic vision) and subjects. In the periphery, 10% cone-silent contrast was visible to all of peripheral tetrasensitivity in the three cone classes in high three subjects. These results indicate that healthy humans possess four photopigments mediate light (photopic vision). The peripheral tetrasensitivity. peripheral retina sensitivity. identification of a photopigment Our data do not address the (melanopsin) within the retinal question of color appearance. ganglion cell layer was a surprising and significant discovery that If the signals initiated by the four photopigments are represented took place a decade ago. Since that time, melanopsin has been by only three distinct neural populations that code color appear- routinely described as a “nonvisual pigment,” perhaps to high- ance, trichromatic theory may still explain color perception. light its role in functions including pupil dilation and circadian However, tetrasensitivity is necessary to explain peripheral rhythms. However, there is no clear evidence showing that light sensitivity. We also considered whether the fourth photo- melanopsin absorptions are perceived by healthy human sub- pigment might be the rod photopigment, rhodopsin, which is also jects. Coupling psychophysical measurements of light sensitivity absent in the central fovea. Because the visual thresholds were with computational analyses, we report that absorptions from measured on a very intense mean background (2,060 cd/m2), thi- a fourth photopigment, probably melanopsin, are required to s explanation is inconsistent with many estimates of rod sensitivity explain visual sensitivity outside of the fovea. These findings on bright backgrounds. Therefore, we think the most likely can- require that trichromatic theory be amended. didate for the fourth photopigment is melanopsin. To test the theory, we took advantage of two key ideas. First, Some melanopsin-containing retinal ganglion cell axons do we suppose a system encodes light using only three types of project to the lateral geniculate nucleus (4), and diseased sub- photopigments, and we present a stimulus that is the sum of jects with complete cone dystrophy are able to detect some four primary lights. In this scenario, there will be many mixtures light (5). Hence, there was reason to suspect that melanopsin of the four primaries that exert the same effect on the three signals might contribute to healthy human vision. To date, the photopigments. Now, we consider two lights that have the same data we present are the strongest evidence for the detection of effect on the three pigments. The difference between these melanopsin-initiated absorptions and a confirmation that mela- two lights is not detected by the cone photopigments, and this nopsin absorptions are perceived by healthy human subjects. difference is a “cone-silent” stimulus (Fig. P1). Modern color science has accurate knowledge about the 1. Newton I (1704) Opticks: A Treatise of the Reflections Refractions, Inflections and Colours properties of the three types of cone photopigments, and we of Light (Printed for William Innys at the West End of St. Paul’s, London), 4th Ed. can make a precise prediction of cone-silent stimuli. One way 2. Young T (1802) On the theory of light and colours. Phil Trans R Soc Lond 92:12–48. 3. Wandell B, Silverstein L (2003) Digital color reproduction. The Science of Color,ed to test for the presence of a fourth photopigment is to present Shevell S (Optical Society of America, Washington DC), 2nd Ed. subjects with cone-silent stimuli and determine whether the 4. Dacey DM, et al. (2005) Melanopsin-expressing ganglion cells in primate retina signal subject can see such a stimulus. If the subject perceives cone- colour and irradiance and project to the LGN. Nature 433(7027):749–754. silent stimuli, we must conclude that a photopigment apart 5. Zaidi FH, et al. (2007) Short-wavelength light sensitivity of circadian, pupillary, and from the cone photopigments contributes to vision. visual awareness in humans lacking an outer retina. Curr Biol 17(24):2122–2128. Any such experiment must assess the accuracy of the meas- urements and account for biological variability in the various pigments within the living human eye. To assess the ability of our Author contributions: H.H., J.W., and B.A.W. designed research; H.H. and R.F.D. per- methods to account for these variations, we took advantage of formed research; H.H. and R.F.D. contributed new reagents/analytic tools; H.H. and J.W. analyzed data; and H.H., J.W., and B.A.W. wrote the paper. another important feature of the human retina: The central fl visual field is free of the melanopsin photopigment. If mela- The authors declare no con ict of interest. nopsin absorptions can be perceived, we expect trichromacy to This article is a PNAS Direct Submission. predict visual sensitivity in the fovea but not in the periphery. 1To whom correspondence should be addressed. E-mail: [email protected]. Hence, we compared measurements between the central and See full research article on page E260 of www.pnas.org. peripheral fields within the same observer. Cite this Author Summary as: PNAS 10.1073/pnas.1214240110. NEUROSCIENCE www.pnas.org/cgi/doi/10.1073/pnas.1214240110 PNAS | January 15, 2013 | vol. 110 | no. 3 | 823 Downloaded by guest on October 2, 2021.
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