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Copyright 2001 Psychonomic Society, Inc. 244
Psychonomic Bulletin & Review 2001, 8 (2), 244-
The recent growth of molecular genetics research has
generated much interest in the relations between genetic
potentialities and human behaviors. Although investigat-
ing such relations are fraught with many complexities and
important ethical considerations, there are some cases in
which the linkage between genes and physical realization
is relatively straightforward. One such case is that of the
genetic basis of human color perception.
This paper investigates the linkages between individ-
ual’s genetic potential for possessing retinal photopig-
ments (or the visual pigments responsible for color per-
ception) and individual color perception differences. We
begin by introducing some concepts and terminology
that will be used throughout this paper. Next, we review
recent key findings in molecular genetics research on ret-
inal photopigment opsin genes. Related results from color
perception psychophysics and color and cognition research
are then described. Finally, we describe an analysis of color
vision genes and present new results from an experiment
that investigated the connection between photopigment
opsin genes and color perception. We discuss the results
of this new research as related to existing color perception
theories, as well as the implications for psychological stud-
ies of color processing.
To begin, a brief review of the molecular genetics under-
lying the biological bases of color vision, including de-
fining terms and concepts, is in order. Concepts and terms
are simply defined now and are discussed in detail later
on. Interested readers can find additional material in Mol-
lon (1995), Nathans (1997), M. Neitz and J. Neitz (1998),
and Zegura (1997).
In the present paper, we investigate photopigment opsin
genes , which are simply defined as the genetic sequences
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
retina that respond maximally to specific portions of the
visible electromagnetic spectrum. Three general classes
of photopigments are known to exist: those most sensitive
to the short-wavelength region of the spectrum (abbrevi-
ated SWS cones), those most sensitive to the middle-
wavelength region (MWS cones), and those most sensi-
tive to the long-wavelength region (LWS cones).
Due to the intricacies of gene expression mechanisms,
people who possess the genetic code for the three classes
of photosensitive retinal cones may or may not “express”
Portions of this research were presented at the 1998 European Con- ference on Visual Perception, the 1998 meeting of the Optical Society of America, and the 1998 meeting of the Psychonomic Society. Partial support was provided by the National Science Foundation (Grant NSF- 9973903 to K.A.J.) and a UCSD Hellman Faculty Award (to K.A.J.). The authors acknowledge the many helpful suggestions made on earlier versions of this manuscript by G. Paramei, L. Hurvich, R. Mausfeld, S. Link, R. M. Boynton, D. I. A. MacLeod, V. Bonnardel, R. G. D’An- drade, N. Alvarado, L. G. Carrera, and K. Goldfarb. Correspondenc e should be addressed to K. A. Jameson, Department of Psychology, Uni- versity of California at San Diego, 9500 Gilman Dr., La Jolla, CA 92093- 0109 (e-mail: [email protected]).
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 literature shows that gender-linked differences in color perception
warrant further investigation of retinal photopigment classes and color perception relations. We use
genetic analyses to examine an important position in the gene sequence, and we empirically assess and
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.
RICHER COLOR EXPERIENCE 245
all three classes in their retinas. For example, a person with
gene sequences for SWS, MWS, and LWS cone types may
express, or physically manifest, only two of those types
retinally (e.g., SWS and MWS cones). Thus, each person
has a genotype (i.e., the genetic potential, or genes, pre-
sent in their DNA) and a phenotype (i.e., the realized
manifestation, or expression, of genetic potentialities in
their genetic code). Thus, the phenotype need not be a
full representation of the genotype.
The three classes of photopigments respond to visible
light and are generally believed to transmit their signals
into a postreceptoral neurally trivariant processing sys-
tem (MacLeod, 1985). This defines the three-channel
color signal processing called trichromacy , which gov-
erns perceptual behaviors such as color matching. Tri-
chromacy, then, is a theory of color perception based on
three receptor classes that feed into three neural channels
and that ultimately produce the rich system we experi-
ence as color percepts (see Brindley, 1960, pp. 198–221,
for further discussion of the three-receptor hypothesis).
A fact that complicates research on this issue is that
the only certain method for exactly determining a per-
son’s expressed phenotype is to directly examine the
retina through “invasive” methods such as microspectro-
photometry or in vivo imaging (Roorda & Williams,
1999). Thus, although tests for color vision abnormali-
ties exist, are widely used (e.g., anomaloscope color-
matching and pseudoisochromatic-plate tests), and are
fairly accurate in classifying some phenotypes that arise,
they are not designed for determining what cell classes
are actually expressed in an individual’s retinas. In any
case, enough can be shown to prove that people exist
who are trichromats (i.e., with trivariate color vision), who
are dichromats (i.e., lacking one of the three standard
signals of color experience, also called color-blindness ),
and who are anomalous trichromats (with trivariate color
vision but with an anomalous shift in the sensitivity in ei-
ther the LWS or MWS systems).
Shifts in sensitivity found in anomalous trichromats
can occur as the result of naturally occurring amino acid
mutations (or polymorphisms ) in specific locations (or
codons ) of the gene sequence of a given retinal photo-
pigment class. In such cases, a person may, for example,
have normal (or wildtype ) SWS and MWS genes but may
have a mutated LWS gene (or LWS-photopigment poly-
morphism ) that produces the shift in that cone class’s re-
sponse sensitivity. Polymorphisms of this sort occur rather
frequently on MWS and LWS gene sequences and thereby
add to the variety of possibly expressed retinal pheno-
types in a given population.
It is also possible for a person to possess both a poly-
morphic variant for a given cone class and the gene se-
quence for the wildtype, or normal, variant of that same
photopigment class. In effect, such people possess the
genetic potential for two variants of the same photopig-
ment class, with peak sensitivity at different (albeit very
close) spectral frequencies. Such people when female are
called heterozygotes , and, below, we assess and review
some possible consequences of heterozygote perception.
THE BIOLOGICAL BASIS
OF TRICHROMACY
We start with a review of recent findings relevant to the
perception of people possessing more than three classes
of retinal cones. The linkage between color perception
phenomenology and the neurophysiological basis of color
vision has generated an impressive record of psycholog-
ical and biological research. The 19th century Young–
Helmholtz three-component theory developed the idea
that color vision is trichromatic due to the presence of three
retinal visual pigments, or “photopigments” (see Brind-
ley, 1960). Genetic research showed that color vision is
a sex-linked trait, because the genes coding for long-
wavelength-sensitive (LWS) and medium-wavelength-
sensitive (MWS)^1 photopigments are X chromosome in-
herited,^2 and the genetic sequences associated with these
photopigments were isolated (Nathans, Piantanida, Eddy,
Shows, & Hogness, 1986; Nathans, Thomas, & Hogness,
1986). Further work determined that genotypes involving
more than three photopigment opsin variants are com-
mon and that mechanisms governing the expression of
such photopigment opsin genes allow for the possibility
of an individual expressing more than three retinal pho-
topigment types (Dartnall, Bowmaker, & Mollon, 1983;
Merbs & Nathans, 1992a; Mollon, 1992, 1995; J. Neitz
& Jacobs, 1986; J. Neitz, M. Neitz, & Jacobs, 1993;
Winderickx, Battisti, Hibiya, Motulsky, & Deeb, 1993).
Recent studies show that these commonly occurring
genetic polymorphisms produce variations in spectral tun-
ing of expressed photopigments. Such spectral shifts are
attributable to amino acid substitutions at specific loca-
tions in the opsin gene (Deeb & Motulsky, 1996). The
X-linked inheritance feature, when coupled with the pos-
sibility of opsin gene polymorphisms, allows for a con-
siderable percentage of females to be heterozygous at cer-
tain critical amino acid positions for MWS or LWS opsin
genes. That is, females who possess two distinct genetic
variants at certain codons (with one variant on each of
two X chromosomes).^3 Previous research proposed that
such genetic heterozygosity may have perceptual conse-
quences in individuals who actually express all four types
of photopigment genes, because each gene type produces
different retinal photopigment sensitivities, in effect yield-
ing a four-cone-class retinal phenotype (Deeb & Motul-
sky, 1996; DeVries, 1948; Jordan & Mollon, 1993; Krill &
Beutler, 1965; Mollon, 1992; Nagy, MacLeod, Heyne-
man, & Eiser, 1981; Schmidt, 1955).^4
A few investigators have conjectured that some indi-
viduals who possess four photopigments in their retinas
might have a dimension of perceptual experience that is
not experienced by trichromat individuals (Deeb & Mo-
tulsky, 1996; Mollon, 1992, 1995).^5
As discussed by Cohn, Emmerich, and Carlson (1989)
heterozygous females fail to be detected by the use of an
anomaloscope, although there are reported shifts in their
anomaloscope color matches (Crone, 1959; Feig & Ropers,
1978; Krill & Beutler, 1964; Pickford, 1959; Schmidt, 1955),
as well as shifts using flicker photometry (Crone, 1959; Ya-
RICHER COLOR EXPERIENCE 247
lengths (Hsia & Graham, 1957; Wilder, 1970).^9 Also, Vl of
protanope individuals peaks at shorter wavelengths, rela-
tive to the trichromat Vl , and exhibits a gross loss of sensi-
tivity in the long-wavelength spectral region (Hecht &
Shlaer, 1936; Hsia & Graham, 1957; Wilder, 1970). Re-
cent research suggests that updating normative cone fun-
damentals to reflect dichromat subgroup differences would
provide a more appropriate model of the dichromat color
response (Sharpe, Stockman, Jaegle, et al., 1998; Stockman
& Sharpe, 1998). Thus, the accepted normative model of
responsivity to natural daylight ( i.e., Vl ) may accurately
describe the trichromat response, but it does not, as previ-
ously thought, completely generalize as a model of dichro-
mat photopic luminosity response. In view of these find-
ings, it seems reasonable to consider the impact that
four-pigment retinal processing might have on accepted
standards of Vl and normative cone fundamentals.
A related aspect of color perception and cognition be-
havior is the manner with which individuals categorize
and name their color perceptions. Color vision capabili-
ties are believed to be developed and functioning equally
in males and females by 1 year of age. In 5- to 6-year-old
children, the ability to identify primary colors by name is
significantly greater in girls than in boys (although no sig-
nificant difference is found in the same subjects for draw-
ing geometric designs). The explanation offered is that
“various constitutional and environmental factors un-
doubtedly influence the acquisition of color-naming
ability by children,” and “verbal skill and interest in col-
ors may vary between boys and girls” (Anyan & Quillian,
1971, p. 1631). In adults, a number of studies suggest that
color lexicons differ in fundamental ways across gender
(Lakoff, 1975; Nowaczyk, 1982; Rich, 1977; Swaringen,
Layman, & Wilson, 1978; Thomas, Curtis, & Bolton,
1978). Comparative cross-cultural studies of some Asian
cultures found that females prefer reddish, pink, and pur-
plish colors (Saito, 1994, 1996, 1999).
Furbee et al. (1997) reported gender differences in
color naming between males and female subjects. In a
study of triadic comparisons of color-sample judged sim-
ilarity, they found that males and females are differenti-
ated by empirically defined two-dimensional and three-
dimensional similarity structures. Specifically, females
were found to more strongly represent a red-to-yellow-
to-green dimension relative to their male counterparts
(who were negatively correlated with that dimension).
This finding suggests that an increased dimensionality
in the scaling solution is needed to adequately capture
the female representation of color similarity.
These kinds of differences (which are in opposition to
a model of shared, pan-gender visual processing mech-
anisms) went unnoticed or were attributed to possible
gender differences in socialization (e.g., Anyan & Quil-
lian, 1971). Gender differences were not a focus of study
for much of the work on the cognition and categorization
of color (see Hardin & Maffi, 1997, for a review), quite
simply because, heretofore, gender differences were not
suspected as a differentiating factor in color perception.
The interesting question at hand is whether our new
understanding of the photopigment opsin genotype–
phenotype relation warrants a reexamination of the color
perception of people with four-photopigment retinas.
What aspects of their perceptions may differ from those
of trichromats? And, is this X-chromosome-linked geno-
type the basis of the gender-based differences in color
processing that have been observed in the psychologi-
cal literature thus far? A substantiated gender-specific
genotype perceptual relation would represent an impor-
tant consideration for most psychological studies of
color and cognition, including those investigating the
dimensionality of color perception space, color memory,
color-naming behaviors, and, more generally, color lex-
icons.
On the basis of the results reviewed above, the present
research examines the color perception of individuals ex-
hibiting the genes for four-photopigment retinas. The re-
sults are compared with those of individuals exhibiting
both the genes and color perception of “normal” three-
photopigment retinas and def icient two-photopigment
retinas. The aim is to determine whether an experimental
task that extends the stimulus complexity beyond the color-
matching configuration might reveal X-chromosome-
based color perception differences previously undetected
in the standard psychophysical tasks. Such an investiga-
tion necessarily consists of two distinct components: a
laboratory analysis of subjects’ photopigment opsin genes
and a behavioral test of subjects’ color perception. These
two components are now described.
ANALYSES OF PHOTOPIGMENT
OPSIN GENES
The goal of our photopigment opsin genes analyses is
to specify the genetic potential of participants in our color
perception study. Issues underlying the crucial genetic
differences in photopigment opsin genes require a con-
siderable amount of explanation. Appendix A details our
rationale and methods and emphasizes that, relative to
males and females who have the expected gene sequence
(at codon 180) for LWS and MWS genes, the females
who have both amino acids (alanine and serine) at codon
180 possess more diverse opsin genes underlying photo-
pigment expression in the retina. As implied above, the
interesting question is whether this increased variety of
photopigment opsin genes produces differences in color
perception in individuals possessing such genes. Inves-
tigating this genotype/perceptual–phenotype relation ne-
cessitates both a genetic analysis of subjects DNA and an
empirical assessment of those subjects’ color perception.
Genetic analyses reported now are followed by a de-
scription of the behavioral experiment conducted.^10
Method
Subjects. Sixty-four University of California, San Diego, sub- jects volunteered through the psychology human subject pool for partial course credit, were solicited by advertisement and partici-
248 JAMESON, HIGHNOTE, AND WASSERMAN
pated for cash payment, or were volunteers for research participa- tion. DNA specimens from each subject were analyzed in a manner following existing research using standard procedures described in detail in Appendices A and B. On the basis of blind polymerase chain reaction (PCR) genetic assays, 64 subjects were partitione d into the six genotype groups seen in Table 1.
Results
Table 1 presents the results from PCR genetic analysis
of 64 subjects. These results were further refined by re-
sults from standard color vision screening methods using
the Ishihara Pseudo-Isochromatic Color Plates and the
Farnsworth–Munsell 100-Hue Test.^11 Together, the ge-
netic analysis and the color vision screening results of
our subjects allow the determination of the subject par-
titions given in Figure 1. Figure 1 schematically depicts
the genotype–phenotype classifications of our sample of
64 subjects. Figure 1 relates gender partitions to identi-
fied genotypes and relates genotype to the predicted phe-
notype partitions (Figure 1, left column). All predicted
phenotype partitions were defined genotypically and,
when possible (i.e., for trichromat and dichromat parti-
tions only), were also verified using standardized percep-
tual tests. Existing color vision screening tests are not ap-
propriate, given the heterozygote’s potential for deviation
beyond trichromacy, for confirming the heterozygote
partition.^12
Genetic analyses (summarized in Table 1) and the
subject classification scheme (represented in Figure 1)
yield the identification of three subject partitions.
These are (1) subjects who are likely expressors of four-
photopigments in their retinas (i.e., 23 female heterozy-
gotes), (2) those likely expressors of three-pigment retinas
(i.e., 22 male and 15 female functioning trichromats), and
(3) those who may possess the genes required for three-
pigment retinas but who, due to a genetic expression event,
function as if they possess only two retinal photopigments,
as indicated by unequivocal failure in standard color vision
screening (i.e., 4 functionally dichromat males).
The subjects depicted in Table 1 and Figure 1 also par-
ticipated in a color perception experiment. The experi-
ment was designed to serve three aims: (1) to go beyond
the limitations found in standardized color vision screen-
ing, (2) to evade the assumptions of trichromacy inher-
ent in methods that primarily isolate metameric equiva-
lence mechanisms (e.g., Rayleigh matching), and (3) to
make use of contextually rich viewing conditions that in-
Table 1 Sixty-Four Subjects Classified by PCR Analyses of Red and Green Gene Codon 180 Amino Acid Sequences
Amino Acids Identified Possible Configurations of Photopigment Genotypes Suggested by Retinal Photopigment in Codon 180 Phenotypes of Amino-Acids Amino Acids on Codon 180 of the Likely to Arise Given the PCR Tests on X 1 2 X 2 or X 1 Red and Green Opsin Gene Arrays Codon 180 Results Serine and Alanine (Ser)X 1 2 (Ala)X 2 XSer: Nrml.R. gene and (a) Nrml.R.+ Ab.R. Female ( n 5 23) (Ala)X 1 2 (Ser)X 2 XAla: Ab.R. gene (b) Nrml.R.+ Nrml.G. or : Nrml.G. gene (c) Nrml.R.+ Ab.R.+ Nrml.G. or : Ab.R. and Nrml.G. gene Alanine Female (Ala)X 1 2 (Ala)X 2 XAla: Ab.R. gene (d) Ab.R. ( n 5 7) or : Nrml.G. gene (e) Nrml.G. or : Ab.R. and Nrml.G. gene (f ) Ab.R.+ Nrml.G. Serine Female (Ser)X 1 2 (Ser)X 2 XSer: Nrml.R. gene (g) Nrml.R. ( n 5 8) Alanine Male (Ala)X 1 XAla: Ab.R. gene (h) Ab.R. ( n 5 14) or : Nrml.G. gene (i) Nrml.G. or : Ab.R. and Nrml.G. gene ( j) AB.R.+Nrml.G. Serine and Alanine (Ser+Ala)X 1 XSer+Ala: Nrml.R. gene and Nrml.G.gene (k) Nrml.R.+ Nrml.G. Male ( n 5 5) or : Hybrid Nrml.R. + Nrml.G. gene (l) Nrml.R. or : Hybrid Nrml.R. + AB.R. or : Hybrid Nrml.R. + AB.R. and Nrml.G. gene Serine Male ( n 5 7) (Ser)X 1 XSer: Nrml.R. gene (m) Nrml.R.
Note—Abbreviations as follows: Nrml., normal; AB., abnormal; R., red; G., green. X 1 denotes a single X chromosome, and X 2 denotes a second X chromosome. Column 1 presents subject types grouped by PCR analysis results at codon 180 of the red and green photopigment opsin genes (described in Appendi x B). Column 2 suggests the arrangement of amino acids (serine or alanine) on the available X chromosomes for the males and females tested. Column 3 details the photopigment opsin genes most likely arising from the amino-acid sequences identified on the available chromosomes. Column 4 presents possibly occurring photopigment phenotypes given the present genotype analysis. (Phenotypes in column 4 do not include information on the short-wavelength-, or blue-, sensitive pigment gene.) Appendix A provides details of the genotype classification procedure. Note that only one phenotype listed in column 4 involves the expression of two LWS photopigments plus one MWS photopigment [Case (c) of the serine + alanine female group]. Any of the other possible phenotypes listed either have fewer photopigment classes expressed or have the same number of photopigment classes [(f), ( j), and (k), which, compared with the probability of expressing (c) or (a) of the heterozygote geno- type, are estimated to occur as an expressed phenotype less frequently, given the phenotypes possible within those respective genotypes]. Table 1 presents the most general analysis regarding the codon 180 genotype–phenotype relation. Further complexities arising from gene number, X in- activation, and other expression mechanisms continue to be studied by molecular geneticists and await specification for the opsin genes. Although the subject group partitions characterized in Table 1 will likely become more complex with further analyses of genetic mechanisms (e.g., the spec- ification of detailed differences implied by MWS gene serine 180, the expression of a greater number of pigment genes from a single X chromo- some, or the unresolved expression consequences of chimeric, or hybrid, genes), our crucial assertion that serine + alanine females will exhibit a more diverse opsin genotype and will possess the genetic potential to phenotypically express more kinds of retinal photopigment classes relative to the other subject classes identified here will remain unchanged.
250 JAMESON, HIGHNOTE, AND WASSERMAN
For example, concerning the width of the subject’s percept (or per- ceived “gamut”), two separate tasks instructed the subject to “Mark the Right [or Left] extreme edge of the rainbow.” Regarding the num- ber and location of distinct chromatic bands (a.k.a. “delineations ”) the subjects responded to eight different task instructions, including “Mark all the edges for all the bands of color in the rainbow,” and “Starting from the Left [or Right] side of the display carefully count to the 1st [or 2nd,... , or 7th] band of color and mark both edges of the 1st [or 2nd,... , or 7th] band of color.” Finally, seven different instructions regarding to the location of best-exemplar appearance s were used: “Indicate by a single mark the position of the Best Ex- ample of Violet [or Blue , Green , Yellow , Orange , Red , or Purple ] in the rainbow.” Data from three types of judgments are presented here: (1) the task in which the subjects were instructed to demark “all the edges for all the bands of color in the rainbow” (hereafter called “delin- eation data”), (2) the task in which the subjects indicated the loca- tion of the best-exemplar appearance for several color categorie s (called “best-exemplar data”), and (3) the task in which the subjects were instructed to “mark the Right [or Left] extreme edge of the rainbow” (called “perceived gamut” data). Each subject’s delinea- tion data were based on six repetitions of this task. Each subject’s best-exemplar locations were based on three judgments per each color categor y. Each subject’s perceived gamut data were based on three judgments per edge. All judgments were randomly presented within the experiment ’s 80 total trials. All subjects were given a different random order of stimuli. Each trial sequence was terminated by actuating a photographic flash, which created an energy mask designed to eliminate stimulus after-
images from trial to trial. Between trials, the stimulus was shielded from view by a closed aperture, and the room ambient remained dark while the experimenter (1) set up the response sheet for the next trial, (2) established a calibration mark for the trial, and (3) ex- plained the next task to the subject. Each trial required an estimated ~10–30 sec to complete, with an estimated intertrial interval of ~20–60 sec. The physical attributes of the projected display were constant from trial to trial; however, in debriefing, some subjects re- ported uncertainty regarding whether stimulus manipulations were made across trials. Following the experimental session, subject s were screened for color vision deficiencies using the Farnsworth– Munsell 100–Hue Test and Ishihara Pseudo-Isochromatic Color Plates (11th ed.). We assume that the ability to perceive and delineate bands of chromatic difference along the spectrum is a function of the detec- tion and discrimination of noticeable differences in spectral wave- lengths (cf. Boynton, Schafer, & Neun, 1964; Smeulders et al., 1994). Thus, the relation between photopigment genotype and performance in the spectral delineation task is hypothesized to be that increases in classes of expressed photopigments impact detection and discrim- ination in such a way as to produce increases in the number of chro- matic bands perceived and delineated in the diffracted spectrum. Regarding a subject’s placement of best-exemplar locations in the spectrum, we made the conservative prediction that the data would be comparable to the spectral locations of unitary hues investigate d in previous studies (Boynton et al., 1964; Dimmick & Hubbard, 1939; Purdy, 1931; Westphal, 1910, cited in Boring, 1942). The ra- tionale for this was the following: First, because unitary-hue (or best-exemplar) locations in anomalous trichromats and “normal” trichromats were previously found to be similar for the percepts of blue, green, and yellow, we expected our subjects’ data to display a similar agreement. Second, we expected to observe substantial in- dividual variation in best-exemplar locations within all of our sub- ject partitions. Third, we expected that individual variation in some cases would exceed the differences observed between our groups’ average locations. Thus, we predicted reasonable correspondence s between all our subjects’ best-exemplar locations and the spectral locations of unitary hues found in existing research. Data analysis. As mentioned above, the present analyses exam- ine for each subject (1) the total number of bands delineated in the diffracted spectrum display (six repeated observations per subject), (2) the locations of the best example of the individual colors red, or- ange, yellow, green, blue, violet,^14 and purple (three repeated ob- servations per color for each subject), and (3) the locations of each extreme edge perceived in the stimulus (three separate observation s per edge, left and right extreme, per subject). All subjects’ response s were processed blind and verified for measurement and recording accuracy by two independent experimenters. Unless otherwise stated, all tests of significance reported use two-tailed Student’s t tests for unequal samples. All reported tests of significance on mean mea- sures were also verified by appropriate tests on medians.
Results
Delineation of spectral chromatic bands. Our first
hypothesis was that the subjects expressing more than
three photopigments would have a different phenome-
nological color experience. This could be demonstrated
in the ways they segment the chromatic components of
the diffracted spectrum. Thus, people with four photo-
pigments are expected to experience more chromatic
“bands” in the rainbow than are trichromat or dichromat
individuals. Similarly, trichromat individuals should ex-
perience more bands than should dichromats. With respect
to behavioral measures, the general prediction is that the
genetic potential to express more than three photopig-
Figure 2. Experiment 1 apparatus and materials. The light source employed was a 500-W halogen lamp (1) with a broad spectrum energy component extending beyond the 400 to 700-nm range and with a substantial component in the long-wavelength end of the spectrum. A rectangular aperture (2) was used as an image plane for collimating the source, and an iris (3) was used to minimize scattered light. Collimated light from lens 4 impinged on a blazed diffraction grating (6) and was controlled by an in- tervening switch activated aperture (5). Lenses (7 and 8) were used to form a magnified image of the diffracted spectral image reflected off the grating (6). This image was back-projected onto the Lucite panel (9) and viewed binocularly by subjects. Inter- trial energy masking was achieved using a photography flash (10). The entire apparatus depicted in this figure was configured within a 3 3 3 foot area (drawing is not to scale).
RICHER COLOR EXPERIENCE 251
ments is correlated with an observed increase in the num-
ber of chromatic bands perceived and delineated in the
diffracted spectrum.
Table 2 summarizes the results for the subject parti-
tions depicted earlier in Figure 1 (four-photopigment fe-
males, trichromats, and dichromats). Table 2 also includes
data from a subpartition of only trichromat females. Mean
number of spectral delineations, standard deviation, and
sample size for these four groups are presented. The data
in Table 2 confirm that the number of spectral bands that
a subject delineates systematically varies with the MWS
and LWS photopigments that a subject is presumed to ex-
press. As one would predict from trichromatic theory, di-
chromat individuals (in this case, protanopes) delineate
significantly fewer ( p < .05) chromatic bands than do tri-
chromats (5.3 vs. 7.3). The number of bands delineated
by our four-pigment females (i.e., heterozygotes) and by
our male and female trichromat subjects (10 vs. 7.3) is also
significantly different ( p < .01). Interestingly, male tri-
chromats ( n 5 22) and female trichromats ( n 5 15) were
not significantly different regarding the number of chro-
matic bands each group on average delineates ( p 5 .44).
These results show that, in the present task, photopig-
ment genotype predicted the number of chromatic bands
a subject perceives, in that increases in perceived chro-
matic bands were found with increases in retinal photo-
pigment opsin genes. Moreover, the subjects with four-
photopigment retinas perceived signif icantly greater
numbers of chromatic appearances than did the subjects
with trichromat retinas. Also, consistent with trichromatic
theory, the male and female trichromat subgroups did not
differ in the number of chromatic appearances they per-
ceived and delineated.
However, the most stringent test of our hypothesis was
between the female trichromatic subjects and the female
four-photopigment heterozygote subjects. As shown in
rows 1 and 2 of Table 2, the mean numbers of bands de-
lineated by the two groups of females (7.6 vs. 10) were
significantly different ( p < .01). This comparison elim-
inated differences in performance attributable to gender
and thus was a stronger test of our hypothesis that having
four pigments yields a perceptual difference. The level of
statistical significance observed indicates that these two
female groups were not samples of the same underlying
population. Overall, Table 2 indicates a systematic rela-
tionship between the observed number of bands delin-
eated by the subjects and the number of photopigments
they are presumed to express. These results suggest that
perceptual color experience for heterozygote females is
more articulated than is color perception for “normal”
trichromatic subjects.
Note that, as can be seen in the Table 2, the four-pigment
females showed much more variability in their judgments
(e.g., SD 5 2.96) than did the other comparison groups
(e.g., SD 5 1.80 for the trichromatic females, and so on).
This is consistent with the notion that four-pigment fe-
males are judging a more varied color percept, since
(1) compared with perceiving only a few chromatic dif-
ferences, finer grained distinctions (under equal levels
of acuity) might produce increased perceptual variation
due to the relative perceptual complexity and the need to
register a greater number of perceptual distinctions, (2) an
empirical task that requires demarkation of greater num-
bers of perceived delineations would be expected to in-
crease the chances for additional error and variability in
judgments, and (3) Poynter (1988) has shown in the gen-
eral population that more variability is found in judg-
ments for different-color comparisons versus same-color
comparisons (i.e., judging brightness of two different
colors vs. judging the brightness of two samples of the
same color). Thus, if our four-pigment females are actu-
ally perceiving a finer gradation of color differences, as
these data suggest, then we might expect their judgments
to contain more variability relative to those groups who
perceive fewer colors in the spectrum.
Finally, the genotype “heterozygote” only probabilis-
tically predicts the expression of a four-pigment pheno-
type. Thus, our heterozygote partition was likely to in-
clude (simply due to genetic expression mechanisms)
some females who were genotypically heterozygous but
phenotypically trichromat. At present, the only definitive
way to determine which heterozygotes unequivocally
possess four classes of retinal photopigments is to exam-
ine biopsied retinal tissue or to use a new method of imag-
ing the retina that is not yet widely available (Roorda &
Williams, 1999). Phenotype variability in our heterozy-
gote partition would necessarily increase the variability
observed in groupwise analyses of data from that subject
partition.
Figure 3 presents the locations of chromatic bands de-
lineated by trichromat females ( n 5 15; bottom panel)
and heterozygote females ( n 5 23; top panel). For each
panel, the subjects are rank-ordered on the vertical axis
according to each individual’s average number of ob-
served delineations. The horizontal axis depicts each
subject’s series of average delineation positions, with red
symbols identifying the beginning of a delineation (or
chromatic band), and blue symbols identifying the limit
of a delineation. Each horizontal series depicted presents
the wavelength location of chromatic bands for each sub-
ject, as related to the color gradient presented at the bot-
tom of each panel, given as a rough approximation of the
Table 2 Mean Number of Perceived Spectral Delineations for Four Subject Partitions Subject Partitions M SD n
(1) Four-pigment females (of heterozygote genotype) 10 2.96 23 (2) Trichromat females 7.6 1.80 15 (3) Trichromats (females and males) 7.3 1.93 37 (4) Dichromat males (protanopes ) 5.3 1.53 4
Note—Classification of subject partition (1) is inferred strictly from genotype analyses identifying heterozygote subjects and (on the basis of results found in existing molecular genetics and microspectropho - tometry research) is probabilistically linked to the four-photopigmen t phenotype (with an estimated 50% incidence of occurrence). Partitions (2), (3), and (4) are based on results from both genotype tests and color vision screening tests. Figure 1 presents the classification scheme for partitions (1), (3), and (4). Partition (2) is a subpartition of group (3) used in comparative analyses.
RICHER COLOR EXPERIENCE 253
experimental stimulus. Diffraction (as opposed to re-
fraction) of the spectrum permits the approximation of
wavelength by a regression line of measured wavelength
against 25 metric distances equally spaced across the
stimulus range. Comparing the density and location of
symbols across the top and bottom panels illustrates the
manner with which the heterozygotes differ from the fe-
male trichromats in their chromatic banding behavior: In
general, heterozygotes perceived more delineations in
the spectrum and exhibited finer grained discrimination
differences in the interval between approximately 580
and 780 nm.
Figure 3 also compares the responses of the subjects
with Newton’s observation of seven perceptible chromatic
delineations in the spectrum. Among the heterozygotes,
21 (91%) identified a median number of delineations of
seven or more bands, whereas 8 (53%) trichromat females
identified a median number of delineations of seven or
more bands. Regarding Newton’s hypothesized seven
chromatic bands, 4 heterozygotes and 2 trichromat females
exhibited a median number of bands equal to seven.
A univariate analysis of variance for between-subjects
effects of the width (as the dependent variable) of each
subject’s spectral range showed that the tested subject
groups did not differ significantly regarding the individ-
ually perceived width of the diffracted spectrum [ F (3,64) 5
0.465, p 5 .79]. This finding excludes the possibility
that increases in banding are simply attributable to an in-
crease in perceived width of the spectrum by individual
heterozygotes.
Spectral location of best-exemplar appearances.
Our second hypothesis was that the subjects putatively
expressing more than three photopigments would not dif-
fer significantly from the “normal” trichromat subjects re-
garding the placement of best-exemplar locations for red,
orange, yellow, green, blue, violet, and purple appearances
in the diffracted spectrum. Thus, we expected that our
heterozygous females would locate the above-mentioned
appearances in spectral locations similar to the locations
given by the trichromat females and males and that said
locations would agree with existing data on the location
of unitary hue experiences in the spectrum (Boynton et al.,
1964; Dimmick & Hubbard, 1939; Purdy, 1931; West-
phal, 1910, cited in Boring, 1942).
Figure 4 presents the data for the heterozygous females
and the trichromat females regarding the placement of
best-exemplar appearances for the tested hue categories
(red, orange, yellow, green, blue, violet, and purple).^15
In Figure 4, each horizontal series of symbols represents
a single subject’s data for the placement of violet, purple,
blue, green, yellow, orange, and red bands. Data for the
female trichromats ( n 5 15) are displayed in the bottom
panel, and data for the female heterozygotes ( n 5 23) are
displayed in the top panel. The data from both groups
Figure 4. Best-exemplar locations for trichromat and heterozygote females. Similar to Figure 3’s representa- tion, individual subjects from each group are represented horizontally as a series of position locations and are sep- arately grouped as trichromats and heterozygotes within the two presented panels. Note that a comparable de- gree of individual variability in the placement of best exemplars is seen across groups. Individual best-exemplar variability is conveyed by the horizontal spread of points seen in the data columns that define best-exemplar re- gions for violet, purple, blue, green, yellow, orange, and red (from left to right). Groupwise averages for the place- ment of best-exemplar locations (represented by the red symbols) are largely in agreement across the two groups (error bars for the groupwise averages represent 1 standard deviation).
254 JAMESON, HIGHNOTE, AND WASSERMAN
lend support to existing normative data on the spectral
location of hue–wavelength association (presumably based
on purely trichromatic samples) in that the consensus on
the locations of blue, green, and yellow were, respec-
tively, approximations to 481, 539, and 590 nm.^16 In Fig-
ure 4, there is also agreement between both partitions of
female subjects for the average location of the best ex-
emplars of all the tested appearances. That is, both groups’
best-exemplar locations were within one standard devi-
ation of other groups’ average best-exemplar locations.^17
In addition, concerning the location of best-exemplar
positions, we found fairly substantial and equivalent
amounts of individual variation within each of the sub-
ject groups represented. This individual variation was
similar for all colors tested, and it occurred to a similar
degree across all groups. Further implications of this
finding for the general determination of best-exemplar
hues and unitary-hue spectral locations will be discussed
in a forthcoming paper.
The main result of the best-exemplar location analysis
is that, consistent with our prediction, on average the two
groups of females we assessed similarly located the po-
sitions of hue best exemplars in the diffracted spectrum.
This finding indirectly lends confidence to the chromatic
banding result presented above and provides another
possible clue as to why previous investigations of het-
erozygote perception did not find color perception dif-
ferences similar to those we found here in comparisons
of female heteorzygotes with female trichromat controls.
That is, the heterozygotes’ richer color experience may
have gone undetected in previous normative research, be-
cause (at least for the case of best-exemplar data), aggre-
gating heterozygote data can yield results that resemble
that found for trichromat subjects. If the subjects’ geno-
type information were not readily available, one may be un-
able to differentiate these two groups strictly on the basis
of their spectral positions of unitary-hue percepts. An
issue of further interest is what such heterozygous color
perception differences would contribute to existing nor-
mative trichromatic standards (e.g., Vl ). We now discuss
our results in the context of color perception theories.
DISCUSSION
The results presented above indicate that, in the pres-
ent study, female subjects who most likely express four
photopigments in their retinas experience a different per-
cept, in comparison with females who most likely ex-
press three photopigments. We believe that this kind of in-
creased color-differentiation behavior in heterozygote
females has gone undetected because of the empirical
methods used in previous research. In contrast to methods
previously used to assess the putative four-photopigmen t
vision of heterozygotes, our experiment used binocular
viewing of a contextually complex stimulus consisting
of a chromatic gradient of heterogeneous luminance. Al-
though the stimulus configuration used here, due to the
need for empirical control and manipulation, by no means
achieved the viewing complexity present in a “natural”
scene, it was clearly a substantial step closer to real-world
viewing complexity when compared with a Rayleigh
match stimulus configuration.^18 In the present psycho-
physical task, the subjects were asked to judge a rela-
tively complex percept. In essence, visual processing in
the present study most likely required the use of addi-
tional perceptual mechanisms beyond those required by
a classical color-matching task. Although added stimu-
lus complexity increases the number of potential expla-
nations for the variation observed, only explanations ul-
timately based on the serine–180–alanine substitution in
photopigment opsin genes (discussed in Appendix A)
can explain why, in these data, increased spectral delin-
eations should occur only for heterozygous females.
The photopigment sensitivity curves produced by the
serine and alanine opsin variants are believed to be iden-
tically gaussian-shaped with peak response sensitivities
differing by 4–7 nm (Asenjo, Rim, & Oprian, 1994; Mol-
lon, 1995; M. Neitz, J. Neitz, & Jacobs, 1995). Although
4 nm may seem a minor difference, in many instances,
small perturbations in a physical or biological system re-
sults in substantial consequences: For example, peak re-
sponses of MWS and LWS photopigments differ by an
estimated 20–30 nm, but their associated percepts are the
distinctly different sensations of green and red
(MacLeod & von der Twer, 2000). Thus, a reasonable as-
sertion is that the serine/alanine 4- to 7-nm difference in
photopigment sensitivity could produce a phenomeno-
logical effect of two perceptually distinguishable reddish
appearances (Mollon, 1992).
Jameson and Hurvich (1956) originally developed the
now well-established color-opponency theory, which
states that small fixed shifts in photoreceptor spectral sen-
sitivity lead directly to systematic alterations in spectral
response functions for the paired chromatic and achro-
matic opponent response systems. This model has given
predictions that agree with data on the color perceptions
and discriminations of anomalous trichromats and dichro-
mat observers (Jameson & Hurvich, 1956). We believe
an extension of the theory may similarly serve to describe
the perception and discrimination mechanisms govern-
ing the color phenomenology of four-pigment observers.
There has been considerable study of the relationship
between perceived color and spectral wavelength, and,
although there are many variables that effect the appear-
ance of spectral wavelength, the general notion is that
“the relation between the wavelength of spectral radiant
energy and perceived hue is so well known that it is
common-place to talk about [spectral] light as if it were
colored” (Boynton et al., 1964). Even so, there are no ex-
isting theories in the color perception literature that de-
scribe why specific chromatic bands are necessarily per-
ceived by an observer viewing a spectrum. Nor is there
an explanation as to why some colors that are associated
with wavelength are found to be distinguishable at one
location of the spectral continuum but not present at an-
other nearby location.
256 JAMESON, HIGHNOTE, AND WASSERMAN
phasizing color equivalence classes, and the other empha-
sizing color differences. The theory should distinguish
between certain psychophysical techniques using non-
complex viewing circumstances as a test of one mode,
whereas other more general and realistic viewing circum-
stances would be more appropriate in assessing the sec-
ond mode (cf. Poynter, 1988).
We have suggested that one approach toward extend-
ing existing models to account for the perceptual impact
of four-photopigment retinal processing would involve
the refinement of stages in an extended zone theory. Such
an extension would also need to take into consideration
recent results on the mapping of the retinal mosaic in
photoreceptor expression (Roorda & Williams, 1999) and
should also account for the impact of variability in such
factors as observer’s macular pigmentation (Sharpe,
Stockman, Knau, & Jaegle, 1998), optical density of reti-
nal photopigments (He & Shevell, 1995), and so on. Such
factors would presumably affect the color vision of four-
pigment observers in ways similar to that found for three-
and two-pigment observers arising from a known genetic
linkage (He & Shevell, 1995).
Concerning the relations between opsin genotype and
expressed photopigments, one theory of phenotypic ex-
pression (Lyon, 1961) predicts that the retinas of het-
erozygous females will be a swirled or patchy mosaic of
spectrally shifted cells and “normal” cells. Ongoing
molecular biology research on the genetic mechanisms
underlying various male and female retinal phenotypes
will undoubtedly produce more details concerning the
diverse range of possible genotypes and the expression
of photopigment genotypes for both males and females.
At present, four-photopigment female individuals are re-
ported to be rather common, by some estimates occur-
ring in up to 50% of the female population (M. Neitz,
Kraft, & J. Neitz, 1998). It is also the case that an esti-
mated 8% of males presumed to be color “normal” likely
represent a four-photopi gment retinal phenotype (ex-
pressing multiple L-pigment opsin gene variants that
could signif icantly contribute to color vision; Sjoberg,
M. Neitz, Balding, & J. Neitz, 1998). All else being equal,
our results suggest that if such males were tested in the
present study, they would perhaps exhibit an extended
percept relative to “normal” trichromats, similar to our
findings for heterozygote females.
Thus, heightened color discrimination of the kind dem-
onstrated here reflects a difference in color perception
that is correlated with an X-linked inherited trait. This is
a factor yet unaccounted for in the psychological study
of color processing in a large proportion of female indi-
viduals and a smaller, yet sizable, proportion of the gen-
eral male population. The fact that, in our task, female
heterozygotes had a phenomenologically different expe-
rience from our group of trichromat females suggests that
photopigment opsin genotype differences can give rise
to color perception differences in real-world viewing,
while producing negligible differences in psychophysical
experiments using classical methods of color matching.
These differences may prove to be significant for stud-
ies probing models of color vision and color perception
spaces. And they suggest that X-chromosome-linked dif-
ferences in color perception may provide a key develop-
ment in understanding some of the unexplained gender
differences described earlier in color-naming behaviors,
color salience and preference, and other color cognitions.
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RICHER COLOR EXPERIENCE 259
degree than that of normal controls (p. 256). These findings are consis- tent with our suggestion, and accord with our data, that such color vision screening tests may erroneously identify four-pigment females as color deficient due to the theory used to construct the screening stimuli.
- It is essential to note that, although the group of four-pigment het- erozygotes in Figure 1 is strictly a genotype classification, no individ- ual in the trichromat or dichromat partition possess the heterozygotes ’ genetic potential for expressing four photopigments. The overwhelming implication from existing genetics data on nonhuman primates and human retinas (e.g., Kraft, J. Neitz, & M. Neitz, 1998) is that a geno- typic female heterozygote will very likely be an expressor of a four- photopigment retina. However, this cannot be verified in our subjects be- cause physical access to their retinas was not possible; nor is it verifiable through any standard color vision screening test. By comparison, the trichromats and dichromats groups in Figure 1 have both (1) been shown by genetic analysis to have three photopigment genotypes (including anomalous genotypes that are known to produce, with a high probabil- ity, functionally color-blind males) and (2) been shown by standard color vision screening tests to be functionally trichromats and dichromats, re- spectively. Thus, the analysis in Figure 1 makes use of all available and appropriate measures for phenotype determination and necessarily im- poses the mixed genotype–phenotype nomenclature four - photoigment heterozygotes , trichromats , and dichromats for our three subject groups.
- A prismatic spectrum refers to the component rays of light pro- duced by refraction when a broadband source, such as sunlight, is passed through a prism. A more precise way of creating a spectrum of compo- nent rays of light is by using diffraction rather than refraction. The two methods give rise to essentially the same end-product stimulus (i.e., a spectral stimulus appearing as a self-luminous rainbow-like gradient with colors ordered red, orange, yellow, green, blue, etc.), with the ex- ception that, relative to prismatic refraction, the diffracted spectrum has the advantages of being linearly related to wavelength by a relationship precisely specified by the diffraction grating parameters.
- Violet was tested rather than Newton’s indigo because it was pre- sumed that the latter color category might not be as widely known among college undergraduates.
- Figure 4 uses the same metric scale distances computed and rep- resented in Figure 3 described earlier.
- Spectral locations of the additional chromatic appearances tested here (i.e., orange, violet, and purple) have not been widely studied in color vision research (see Dimmick & Hubbard, 1939, p. 245).
- Although the data from our male subject groups are not repre- sented in Figure 4, it is worth mentioning that the trichromat males in general located best exemplars in similar positions as to those located by the two female groups presented and also supported existing data on the spectral locations of unitary blue, green, and yellow. Our dichromat subjects’ best-exemplar location data differed from those of the other tested subjects in ways one would expect given the color vision deficien- cies experienced by the subjects in the dichromat group.
- That is, the stimulus used here is sufficiently rich to activate in- ternal mechanisms that are relatively closer to the mechanisms involved in viewing real-world scenes. By comparison, these mechanisms are si- lent in the Rayleigh bipartite field viewing condition. An aspect that distinguishes our stimuli from the Rayleigh match situation is that our visual scene fulfills an important requirement for the activation of mech- anisms that underlie the perception of real-world scenes—that is, a suf- ficiently high variation with respect to chromatic and luminance codes (as discussed by Mausfeld, 1998, pp. 223–224). There is ample evi- dence that core mechanisms of color perception are activated only if there is sufficient articulation that requires (at least) three degrees of freedom in surface reflectance functions implemented by Maloney (1992) using an algorithm, which, interestingly, requires four types of receptor pa- rameters in the “surface complexity condition.”
- Allowing for the fact that each triple of distinct hue–wavelength sensations experienced by a given trichromat individual will vary some- what from that of any other trichromat individual.
APPENDIX A
Appendix A first describes the rationale for the genetic analy-
sis component of this study and then describes the genotype
variants and possible phenotypes arising when amino acid sub-
stitutions occur on codon 180 of the MWS (green) and LWS (red)
gene sequences.
Genetic Structure Underlying Visual Pigment Variation
Because the molecular structures of the LWS and MWS vi-
sual pigment gene bases are 98% identical to each other, there
are relatively few locations in the amino acid sequences where
the LWS and MWS genes can be differentiated by a genetic test
(Asenjo et al., 1994; Nathans, Piantanida, et al., 1986; Nathans,
Thomas, & Hogness, 1986). For the LWS and MWS pigment
genes, these include only 18 variable amino acid positions (see
Jacobs, 1998, p. 2208). Substitutions of amino acids caused by
differences in the genetic sequence can eventually produce dif-
ferent spectral absorption properties in retinal cones. These “di-
morphic” or “polymorphic” sites are locations in the gene se-
quence where two different amino acids can be alternatively
present. Among these 18 sites of variation, only 7 (at codons 116,
180, 230, 233, 277, 285, and 309) involve amino acid substitu-
tions that produce shifts in spectral absorption of the X-linked
photopigment opsins (Deeb & Motulsky, 1996; Jacobs, 1998).A
One position in particular, position 180 on exon 3 of the LWS
and MWS genes, is one of three positions in the gene sequence
(along with codons 277 and 285 at which LWS and MWS genes
can be uniquely distinguished) where a single amino acid sub-
stitution determines a major portion of the spectral shift between
LWS and MWS color vision pigments (Asenjo et al., 1994). This is
exemplified by the fact that amino acid substitutions at codons
180, 277, and 285 can eventually transform a red-sensitive retinal
photoreceptor into a green-sensitive photoreceptor, and vice versa.
In the present study, we specifically examined this important
codon (serine–180–alanine) of the gene sequence because this
position has the following properties: (1) it is one of the seven
sites where an amino acid substitution or “polymorphism” oc-
curs,A2^ (2) it is believed to produce some of the most substantial
shifts in spectral sensitivity (Asenjo et al., 1994; Merbs &
Nathans, 1993); (3) in general, shifts are readily apparent in
codon 180 of the L-pigments but are either smaller or not de-
tected in the M-pigments as evidenced by the measured spectral
peaks (Asenjo et al., 1994; Merbs & Nathans, 1992b, 1993);
and (4) substitutions occurring at position 180 are likely to yield
the largest L-pigment peak absorption shift (M. Neitz & J. Neitz,
1998). Compared with relatively smaller spectral shifts produced
by changes that occur at other locations in the gene array, the
amino acid substitutions at position 180 play an essential role
in producing individual differences in normal color vision and
also play a role in modulating the severity of color vision de-
fects (M. Neitz & J. Neitz, 1998). Thus, codon 180 is a crucial
site to consider when investigating the impact of shifted-peak
spectral sensitivity on perception.
We examine the presence or absence of amino acid substitu-
tions observed at codon 180 for both red and green opsin genes
simultaneously. What can one infer regarding possible retinal
phenotypes from genetics tests on specific codon 180 amino
260 JAMESON, HIGHNOTE, AND WASSERMAN
APPENDIX A (Continued)
acids in either the red (LWS pigment) or the green (MWS pig-
ment) opsin gene? Although larger sample sizes are needed to
accurately assess the population frequency of the serine–
shift versus the alanine–180 shift, some investigations suggest
that the general Caucasian population shows a ~56% occurrence
for the “normal” serine 180 and a ~44% occurrence of a poly-
morphic mutation alanine 180 for the red pigment gene. By
comparison, the frequency of occurrence for the green pigment
gene is ~96% “normal” alanine 180 and ~4% polymorphic ser-
ine 180 (Winderickx et al., 1993).
Asenjo et al. (1994), M. Neitz and J. Neitz (1998), and Sharpe,
Stockman, Jaegle, et al. (1998), show that the serine amino acid
at codon 180 is primarily linked to the normal red gene, whereas
the presence of alanine at codon 180 can indicate the presence
of a polymorphic (shifted) red photopigment gene, the presence
of a normal green gene, or the presence of both a shifted red and
a normal green gene. Winderickx et al. (1992) suggest that MWS-
pigment gene 180 substitutions of serine for the normal alanine
occurs with far less frequency than in the LWS-pigment gene.
When MWS 180 substitutions do occur, they produce non-
significant shifts in the absorption spectra of M-cone retinal
photopigments (Asenjo et al., 1994).A
At present, the consensus is that, although the resulting spec-
tral sensitivity shifts produced by codon 180 substitutions are
significant for LWS-pigments, they are far less common for
MWS-pigments, and, when present, they yield MWS-pigment
spectral absorption peaks essentially identical to the “normal”
MWS-pigment (M. Neitz & J. Neitz, 1998). For the above rea-
sons, we analyzed subjects’ DNA to specify the amino acids pres-
ent at codon 180 in the red and green genes. We now summa-
rize the resulting genotype variants arising from the presence or
absence of particular codon 180 amino acids and the majority
of possibly occurring phenotypes.
Classifying Photopigment Opsin Genotypes
On the basis of existing findings (Asenjo et al. 1994; M. Neitz
& J. Neitz, 1998; Sharpe, Stockman, Jaegle, et al., 1998; Wind-
erickx et al., 1993; Winderickx et al. 1992), presence of codon
180 amino acid variants for either the red or the green gene al-
lows several possible phenotypes to be expressed. These are sum-
marized as follows:
(1) The presence of serine at codon 180 implies the detection
of a normal red gene (because serine is primarily linked to the
normal red gene at position 180);A4^ and (2) the presence of ala-
nine at codon 180 can indicate the presence of a polymorphic
L-pigment gene (with a substantially shifted peak spectral sen-
sitivity from the normal L-pigment gene), the presence of a nor-
mal M-pigment gene, or the presence of both a shifted red gene
and a normal green gene.
What these scenarios imply for possible phenotype expres-
sion is relatively straightforward when dealing with males who
have only a single maternally inherited X chromosome. In this
case, we know when we observe a male who tests positive for the
presence of both serine and alanine and who possesses a single
X chromosome with at least one normal red gene and with at
least one normal green gene or a mutated red gene (we say “at
least one” because we cannot rule out red and green gene copies
occurring at other sites in the red and green gene sequences since
we do not consider other sites in this analysis).
By comparison, when we observe a male who tests positively
for serine 180, we can infer that this individual has a normal red
gene at codon 180, but not a normal green gene or a polymorphic
red gene at position 180.
Likewise, we would infer that a male with alanine 180 would
have either a normal green gene or a polymorphic red gene at
codon 180, but not a normal red gene at 180.
The same codon 180 analysis for females is complicated by
the fact that, relative to males, females have two X chromosomes
capable of carrying red and green genes at codon 180. In females,
one X chromosome is transmitted via maternal inheritance,
whereas a second X chromosome is paternally inherited.
If we consider a female who tests positive only for the pres-
ence of serine at position 180, the following possibilities are al-
lowed: this female has two X chromosomes, each with one nor-
mal red gene. One copy occurs on codon 180 of the first
X chromosome (X 1 ), while a second identical copy might be
found on codon 180 of the second chromosome (X 2 ). The less
probable scenario is that only one of the X chromosomes has
opsin genes at position 180, and the second chromosome has none
of the described red opsin genes at 180. Regardless of the sce-
nario, this female still has at least one copy of the normal red gene.
Alternatively, consider a female who tests positive for the pres-
ence of the alanine polymorphism at position 180: This female
has two X chromosomes, each with a normal green gene or a
polymorphic red gene at codon 180, but not a normal red gene
at 180 (although we cannot rule out a normal gene occurring
elsewhere on another amino acid position in the red gene array).
Thus, for this female, we observe the presence of a normal green
gene and a mutated red gene on X 1 and copies (or a subset of
copies) of that normal green gene and a mutated red gene on X 2.
Depending on the order of these different genes in the red and
green sequences of X 1 and X 2 , and depending on X inactivation
and other expression mechanisms, this female has the potential
for codon 180 to produce at most a normal green photopigment
opsin and a shifted red photopigment opsin.
Even more varied is the female who tests positive for the
presence of both serine and alanine amino acids at codon 180.
In this heterozygote female, we observe an individual with two
X chromosomes, each with at least one normal red gene and with
at least one normal green gene or a mutated red gene. It is pos-
sible that, for this female, the first X chromosome (X 1 ) could
have a different subset of genes from the second chromosome
(X 2 ). Thus, the this female might possess a normal red gene, a
normal green gene, and a mutated red gene on X 1 (or some sub-
set of these genes); and on X 2 also a normal green gene and a
mutated red gene. Depending on the order of these different
genes in the red and green sequences of X 1 and X 2 and de-
pending on X inactivation and other expression mechanisms,
this serine-180–alanine female has more codon 180 gene com-
binations possible on her two chromosomes than any of those
males or females described above.
Appendix A Notes
A1. The other 11 positions are sites where the amino acid sequence can vary but where such variation does not produce shifts in spectral ab- sorption at the level of the retinal cones. A2. In a study of 45 color abnormal males, Sharpe, Stockman, Jae- gle, et al. (1998) report “except for position 180 the highly polymorphic nature of the amino acids within exon 3 makes it impossible to discern whether any particular exon 3 is derived from a red or a green pigment gene” (p. 10059). While the Sharpe, Stockman, Jaegle, et al. study does not focus on “normal” color vision, male and female, subjects, it does provide results which lend insight and may be generalized in the present study until a more extensive study of color normals is completed. A3. Moreover, according to Sharpe, Stockman, Jaegle, et al. (1998), “among red-green hybrid genes that carry serine at position 180, exon
