We are studying the ways in which the visual system processes the image that is focused onto the retina at the back of the eyeball. In the companion paper to this one, we examined the ways by which vision resolves spatial and temporal variations in stimuli – that is, changes in light and dark across the image; we found significant differences between males and females
In this paper we report on sex differences in color vision. There are several reasons why it is especially interesting to study color vision: color vision may well have the longest history of detailed studies of sensory mechanisms, which means that we have a large background on which to build. Furthermore, we now have an excellent understanding of the genetic bases for the initial steps by which light is converted into a neuronal signal. And some of these bases are sex-linked: color vision depends on three types of cones, some of which are more sensitive to the longer wavelengths of light (L-cones), some to the middle wavelengths (M-cones), and some to the shorter wavelengths (S-cones). The genes coding for two of these cone photoreceptors (L- and M-cones) are carried on the X-chromosome.
Sex differences have been noted for various basic sensory functions. For example, in the auditory system females have better hearing sensitivity than males; these and other differences can be related directly to the masculinizing effects of androgens
]. For the olfactory system, a recent, large review of the literature concluded that, in most cases females had better sensitivity, and discriminated and categorized odors better than males
]. At least for these sensory modalities, and also for taste and somato-sensory sensitivity, females do better than males
Gonadal steroid hormones may be the basis for these sex differences. In rhesus monkeys, many androgen receptors are found on neurons throughout the cerebral cortex, including visual cortex
]. There are similar findings for rats, in whom males have more androgen receptors than females, and these are especially plentiful in primary visual cortex
]. A recent review has reiterated these findings and concluded that in both humans and rats the largest concentration of androgen receptors in the forebrain is in the cerebral cortex and not the hypothalamic and limbic areas associated with reproduction
]: these findings would seem to be general across mammals.
Furthermore, in rats, it is the androgens, and not estrogen, that directly affect development of the visual cortex. Early post-natal cell-death (apoptosis) of the visual cortex is reduced by androgens; as a result males have 20% more neurons in the visual cortex
]. This organizational effect is androgen-specific: early exposure of female rats to androgens (implanted capsules of dihydrotestosterone) led to these effects; early exposure to estrogen (implanted capsules of estradiol) did not inhibit post-natal cell-death
]. Because the genes for the L- and M-cones are on the X-chromosome, females might have a double "dose" of sex-related genes. To compensate for this, one of each pair of X-chromosomes is silenced
]. Furthermore many humans have multiple L- and M-genes – we are polymorphic for these genes
]. And different retinal areas might express different alleles, which would affect the responses of these areas and the brain sites associated with different retinal areas. Moreover, the X-chromosome may have a loading of "male-benefit" genes: thus, any recessive alleles must, of necessity, be expressed in a male
]. Furthermore, some of the sex effects we find could be either organizational or activational and could depend on estrogen rather than testosterone; they could even be due to other sex-related genes
Speculatively, however, the preponderance of testosterone receptors in male brains may be the basis for differences in thalamo-cortical connections: early in development axonal growth towards the cortex is in part guided by projections from cortex to the thalamus
]; and these could be affected by variations in gonadal hormones.
Very few studies of color vision, other than those dealing directly with L- and M-cone genes, look for sex differences. Our focus here is particularly on color appearance. We are not considering, therefore, studies of color vision with cognitive or culture-bound effects: for example, reports that among English speakers, women have a larger vocabulary for describing color stimuli than do men
]; also, some cross-cultural studies show that women's color preferences are not the same as those of men
Color sensations can be described along three separate dimensions: hue, saturation, and brightness. Hue is what is commonly referred to as "color" – red, or yellow, or green. Saturation is how deeply colored is the sensation – compare fire-engine red with a pastel red (pink) – the former is highly saturated, while the latter is less saturated; and white is totally desaturated. Brightness has its ordinary everyday meaning -- stimuli ranging from black through grays to white vary in brightness.
A few of the small number of studies that have dealt directly with color appearance used colored samples (Munsell standard reflectance chips). In one study, a form of Multidimensional Scaling (MDS) was used to find similarities among a set of Munsell stimuli and to derive a form of color space
]. But with these sorts of reflectance stimuli, it is not possible to get a wide range of hues of high saturation, while keeping all at approximately the same brightness. (In Munsell terms, this would mean creating chips of high chroma and high value; for reflecting objects seen on a background, the correct term for "brightness" is "lightness.") Because of the problems with separating the dimensions of these stimuli, the investigators had to place various restrictions on the possible solutions from MDS. The major conclusions were that males placed less weight on inter-stimulus separation along a red-green axis but more on a lightness axis as compared to females. However, as the authors admit, the findings may reflect sex differences in cultural factors relating to range of available color terms and access to them.
As part of a battery of visual tests that we have been applying uniformly for some years to large samples of participants, we use magnitude estimation techniques to measure hue and saturation of flashes of monochromatic lights; the intensities of all of these stimuli were adjusted to make them equal in luminance (approximately equal in "brightness"). Our magnitude scaling methods, derived directly from Hurvich and Jameson
], require participants to assign numbers to the sensations elicited by each stimulus. To do this, we use a strict protocol (described below), whose reliability and validity we have explored quite extensively
]. We used two optical systems: about half the participants viewed the stimuli with their natural pupils (Newtonian-View); for the others, the light from a second optical system was focused through the central 2 mm zone of the pupil (Maxwellian-View); in both cases, the illuminance on the retina was the same.
Our magnitude scaling technique uses a continuous scale to describe the hue and saturation of stimuli. It should be noted that this is fundamentally different from hue-naming in which continuous curves are obtained mostly because participants are not entirely consistent in the names they use from trial to trial. Participants find our magnitude estimation procedure easy, it is highly reliable and rapid -- a complete data set, with all repeats, requires less than one hour. Also, from one set of data we can derive a variety of other functions, such as wavelength discrimination, with the same precision as if that function was the only one being measured
The method is very simple: we ask participants to describe their sensations, but in a highly controlled fashion. The necessary and sufficient terms needed to describe hue completely are Red (R), Yellow (Y), Green (G), and (B)
]; a complete description also needs a term for saturation. Unlike most linguistic terms, the basic color terms have universal denotations
], and therefore can be used to inform us about functions common to the entire species rather than to the vagaries of a particular group’s language (see
] for a review). Of course, a participant's native language must have lexical equivalents for R, Y, G, and B, otherwise they could not perform our task
A term for "brightness" is not needed in our studies because all our stimuli are equated for luminance and are seen against a dark background. Under these conditions there will still be some residual differences in brightness
]; but these differences among stimuli are relatively small, which makes our stimuli approximately equal in brightness. In any case, all participants viewed the same stimuli, so that brightness differences alone should not account for the sex differences we report here.
We present here data gathered with our scaling techniques from large samples of color-normal participants. We find sex differences in color appearance of monochromatic lights across the entire spectrum.
The sex differences are unexpected, partly because, as we note later, there are large inter-individual differences in cone ratios and cone distributions across the retina
]. Despite these variations, human color vision is remarkably similar across the population. And yet despite this overall similarity, there are still small, but very real, sex differences. The mechanisms that determine hue and saturation are cortical, meaning that the neuronal inputs from the thalamus have to be rearranged and re-combined (e.g.
]); much of this may take place in primary visual cortex
]. However, the complete recombination is probably done in several stages: one piece of evidence favoring multiple stages is from an individual who had severe dyschromatopsia (colors were severely washed out and difficult to identify), but without loss of color discrimination
]; see also
]. Furthermore, color appearance probably includes several cortical areas beyond the occipital lobe (e.g.
]). Given the sex differences that we are reporting here, this implies that the 23rd
pair of chromosomes exerts an impact on this re-arranging of the neuronal pathways from thalamus through several regions of visual cortex.