Question

How is it that a single photopigment can give a different response to different wavelengths, yet an organism with only one receptor type (and one variety of photopigment) does not have true color vision?

Answer 1

Photopigments respond differently to different wavelengths, but the neural response of the photoreceptor does not specify wavelength.

Univariance principle: a photoreceptor’sresponse is summarized by one variable that specifies the amount of light absorbed. The problem with univariance is that an infinite set of different wavelength-intensity combinations can elicit exactly the same response from a single type of photoreceptor.

Photoreceptors:

Rods are sensitive to scotopic light levels

•All rods contain the same photopigment molecule.

•All rods have the same sensitivity to variouswavelengths of light.

•Therefore, rods suffer from the problem of univariance and cannot sense differences in color.

•Under scotopic conditions, only rods are active,which is why the world seems drained of colour.

Cone photoreceptors: Three varieties:

•S-cones: Cones that are preferentiallysensitive to short wavelengths (“blue”cones)

•M-cones: Cones that are preferentiallysensitive to middle wavelengths (“green”cones)

•L-cones: Cones that are preferentiallysensitive to long wavelengths (“red” cones)

Color vision depends on three classes of cones that are interleaved spatially into a single layer of photosensitive cells. Therefore, the reconstruction of spectral variations across the scene requires the comparison of signals from cones with different pigments that are sampling somewhat different portions of the retinal image. This sampling strategy succeeds in normal scenes because it relies on the fact that the spectral reflectance varies slowly on the spatial scale of the cones. However, for extended stimuli of high spatial frequency, the grain of the trichromatic mosaic can some-times intrude in visual experience. For example, high frequency black and white patterns appear to contain splotches of color (Brewster, 1832) caused by inability of the visual system to reconstruct color and brightness in-formation from the undersampled or aliased retinal image (Williams and Collier, 1983; Williams, Sekiguchi, Haake, Brainard, & Packer, 1991; Sekiguchi, Williams, & Brainard, 1993).

A similar kind of chromatic artifact occurs with stimuli that are very small. Holmgren (1884) reported that tiny monochromatic flashes of light appear to fluctuate in color, presumably as involuntary eye movements cause each flash to stimulate different cones. Hartridge (1954) found more than three sensations under these conditions and concluded erroneously that there must be more than three kinds of receptors in the retina. Many investigators have subsequently studied the detection and appearance of tiny flashes (Bouman & Walraven, 1957; Krauskopf, 1964; Krauskopf & Srebro, 1965; Ingling, Scheibner, & Boynton, 1970; Williams, MacLeod, & Hayhoe, 1981; Cicerone & Nerger, 1989; Vimal, Pokorny, Smith, & Shevell, 1989; Wesner, Pokorny, Shevell, & Smith, 1991; Otake, Gowdy, & Cicerone, 2000). Both the chromatic aliasing with large stimuli and the fluctuation in color of small flashes of light could provide insight into the fine scale topography of the mechanisms responsible for color vision. While it has usually been assumed that these phenomena reveal the granularity of the cone mosaic, they may also reveal the discrete nature of the postreceptoral microcircuitry for color and spatial vision.

An understanding of the role of the cone mosaic in the fluctuations in color appearance of tiny flashes of light has been hampered for at least two reasons. First, it has not been possible to determine the topography of the three cone classes in the subject’s eye. Second, blur by the eye’s optics has prevented imaging a spot of light on the fovea with an area smaller than that of a dozen or more cones. We have overcome both these problems by using an adaptive optics system (Hofer et al., 2001) that removes blur caused by imperfections in the eye’s optics.

Adaptive optics was to study color fluctuation in the appearance of tiny flashes of light. For five subjects, near threshold, monochromatic stimuli with full widths at half maximum of 1/3 arcmin were delivered throughout a patch of retina near 1 deg in which we also determined the locations of L, M, and S cones. Subjects reported a wide variety of color sensations, even for long-wavelength stimuli, and all subjects reported blue or purple sensations at wavelengths for which S cones are insensitive. Subjects with more L cones reported more red sensations, and those with more M cones tended to report more green sensations. White responses increased linearly with the asymmetry in L to M cone ratio. The diversity in the color response could not be completely explained by combined L and M cone excitation, implying that photoreceptors within the same class can elicit more than one color sensation.