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Richer Color Experience in Observers with Multiple Photopigment Opsin Genes

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Richer Color Experience in Observers with Multiple Photopigment Opsin Genes Psychonomic Bulletin & Review 2001, 8 (2), 244-261 Richer color experience in observers with multiple photopigment opsin genes KIMBERLY A. JAMESON and SUSAN M. HIGHNOTE University of California at San Diego, La Jolla, California and LINDA M. WASSERMAN University of California at San Diego School of Medicine, La Jolla, California Traditional color vision theory posits that three types of retinal photopigments transduce light into a trivariate neural color code, thereby explaining color-matching behaviors. This principle of trichro- macy is in need of reexamination in view of molecular genetics results suggesting that a substantial percentage of women possess more than three classes of retinal photopigments. At issue is the ques- tion of whether four-photopigment retinas necessarily yield trichromatic color perception. In the pres- ent paper, we review results and theory underlying the accepted photoreceptor-based model of trichro- macy. A review of the psychological literatureshows that gender-linked differencesin color perception warrant further investigation of retinal photopigment classes and color perception relations. We use genetic analysesto examine an important position in the gene sequence,and we empiricallyassessand compare the color perception of individuals possessing more than three retinal photopigment genes with those possessing fewer retinal photopigment genes. Women with four-photopigment genotypes are found to perceive significantly more chromatic appearances in comparison with either male or fe- male trichromat controls. We provide a rationale for this previously undetected finding and discuss im- plications for theories of color perception and gender differences in color behavior. The recent growth of molecular genetics research has are then described. Finally,we describe an analysis of color generated much interest in the relations between genetic vision genes and present new results from an experiment potentialities and human behaviors. Althoughinvestigat- that investigated the connection between photopigment ing such relationsare fraught with many complexitiesand opsin genes and color perception. We discuss the results important ethical considerations, there are some cases in of this new research as related to existingcolor perception which the linkage between genes and physical realization theories, as well as the implicationsfor psychologicalstud- is relatively straightforward. One such case is that of the ies of color processing. genetic basis of human color perception. To begin, a brief review of the moleculargeneticsunder- This paper investigates the linkages between individ- lying the biological bases of color vision, including de- ual’s genetic potential for possessing retinal photopig- fining terms and concepts, is in order. Conceptsand terms ments (or the visual pigments responsible for color per- are simply defined now and are discussed in detail later ception) and individualcolor perception differences. We on. Interested readers can find additionalmaterial in Mol- begin by introducing some concepts and terminology lon (1995), Nathans (1997), M. Neitz and J. Neitz (1998), that will be used throughout this paper. Next, we review and Zegura (1997). recent key findingsin moleculargeneticsresearch on ret- In the present paper, we investigatephotopigmentopsin inal photopigmentopsin genes. Related results from color genes, which are simply defined as the genetic sequences perception psychophysicsand color and cognitionresearch responsible for the response properties of the photosen- sitive material (i.e., opsin tuned cis-retinal) in human retinas. Retinal photopigments occupy cone cells in the Portions of this research were presented at the 1998 European Con- retina that respond maximally to specific portions of the ference on Visual Perception, the 1998 meeting of the Optical Society visible electromagnetic spectrum. Three general classes of America, and the 1998 meeting of the PsychonomicSociety. Partial of photopigmentsare known to exist: those most sensitive supportwas provided by the National Science Foundation(Grant NSF- 9973903 to K.A.J.) and a UCSD Hellman Faculty Award (to K.A.J.). to the short-wavelength region of the spectrum (abbrevi- The authors acknowledge the many helpful suggestions made on earlier ated SWS cones), those most sensitive to the middle- versions of this manuscript by G. Paramei, L. Hurvich, R. Mausfeld, wavelength region (MWS cones), and those most sensi- S. Link, R. M. Boynton, D. I. A. MacLeod, V.Bonnardel, R. G. D’An- tive to the long-wavelength region (LWS cones). drade, N. Alvarado, L. G. Carrera, and K. Goldfarb. Correspondence should be addressed to K. A. Jameson, Department of Psychology,Uni- Due to the intricacies of gene expression mechanisms, versity of Californiaat San Diego, 9500Gilman Dr., La Jolla, CA 92093- people who possess the genetic code for the three classes 0109 (e-mail: [email protected]). of photosensitive retinal cones may or may not “express” Copyright 2001 Psychonomic Society, Inc. 244 RICHER COLOR EXPERIENCE 245 all three classes in their retinas. For example, a person with THE BIOLOGICAL BASIS gene sequences for SWS, MWS, and LWS cone types may OF TRICHROMACY express, or physically manifest, only two of those types retinally (e.g., SWS and MWS cones). Thus, each person Westart with a review of recent findings relevantto the has a genotype (i.e., the genetic potential, or genes, pre- perception of people possessing more than three classes sent in their DNA) and a phenotype (i.e., the realized of retinal cones. The linkage between color perception manifestation, or expression, of genetic potentialities in phenomenologyand the neurophysiologicalbasis of color their genetic code). Thus, the phenotype need not be a vision has generated an impressive record of psycholog- full representation of the genotype. ical and biological research. The 19th century Young– The three classes of photopigments respond to visible Helmholtz three-component theory developed the idea light and are generally believed to transmit their signals that color vision is trichromatic due to the presence of three into a postreceptoral neurally trivariant processing sys- retinal visual pigments, or “photopigments” (see Brind- tem (MacLeod, 1985). This defines the three-channel ley, 1960). Genetic research showed that color vision is color signal processing called trichromacy, which gov- a sex-linked trait, because the genes coding for long- erns perceptual behaviors such as color matching. Tri- wavelength-sensitive (LWS) and medium-wavelength- chromacy, then, is a theory of color perception based on sensitive (MWS)1 photopigments are X chromosome in- three receptor classes that feed into three neural channels herited,2 and the genetic sequences associated with these and that ultimately produce the rich system we experi- photopigmentswere isolated (Nathans, Piantanida, Eddy, ence as color percepts (see Brindley, 1960, pp. 198–221, Shows, & Hogness, 1986; Nathans, Thomas, & Hogness, for further discussion of the three-receptor hypothesis). 1986). Further work determined that genotypesinvolving A fact that complicates research on this issue is that more than three photopigment opsin variants are com- the only certain method for exactly determining a per- mon and that mechanisms governing the expression of son’s expressed phenotype is to directly examine the such photopigment opsin genes allow for the possibility retina through “invasive”methodssuch as microspectro- of an individual expressing more than three retinal pho- photometry or in vivo imaging (Roorda & Williams, topigment types (Dartnall, Bowmaker, & Mollon, 1983; 1999). Thus, although tests for color vision abnormali- Merbs & Nathans, 1992a; Mollon, 1992, 1995; J. Neitz ties exist, are widely used (e.g., anomaloscope color- & Jacobs, 1986; J. Neitz, M. Neitz, & Jacobs, 1993; matching and pseudoisochromatic-plate tests), and are Winderickx, Battisti, Hibiya, Motulsky, & Deeb, 1993). fairly accurate in classifying some phenotypesthat arise, Recent studies show that these commonly occurring they are not designed for determining what cell classes genetic polymorphismsproduce variations in spectral tun- are actually expressed in an individual’sretinas. In any ing of expressed photopigments. Such spectral shifts are case, enough can be shown to prove that people exist attributable to amino acid substitutions at specific loca- who are trichromats(i.e., with trivariate color vision), who tions in the opsin gene (Deeb & Motulsky, 1996). The are dichromats (i.e., lacking one of the three standard X-linked inheritancefeature, when coupledwith the pos- signals of color experience, also called color-blindness), sibility of opsin gene polymorphisms, allows for a con- and who are anomaloustrichromats (with trivariate color siderable percentage of females to be heterozygousat cer- vision but with an anomalousshift in the sensitivity in ei- tain critical amino acid positionsfor MWS or LWSopsin ther the LWS or MWS systems). genes. That is, females who possess two distinct genetic Shifts in sensitivity found in anomalous trichromats variants at certain codons (with one variant on each of can occur as the result of naturally occurring amino acid two X chromosomes).3 Previous research proposed that mutations (or polymorphisms) in specific locations (or such genetic heterozygosity may have perceptual conse- codons) of the gene sequence of a given retinal photo- quencesin individualswho actuallyexpress all four types pigment class. In
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