Brian Schmidt

Neurobiological hypothesis of color appearance and hue perception

De Valois and De Valois [Vis. Res.33, 1053 (1993)] showed that to explain hue appearance, S-cone signals have to be combined with M versus L opponent signals in two different ways to produce red-green and yellow-blue axes, respectively. Recently, it has been shown that color appearance is normal for individuals with genetic mutations that block S-cone input to blue-ON ganglion cells. This is inconsistent with the De Valois hypothesis in which S-opponent konio-geniculate signals are combined with L-M signals at a third processing stage in cortex. Instead, here we show that color appearance, including individual differences never explained before, are predicted by a model in which S-cone signals are combined with L versus M signals in the outer retina.

The elementary representation of spatial and color vision in the human retina

The origins of spatial and color vision in the human retina. The retina is the most accessible element of the central nervous system for linking behavior to the activity of isolated neurons. We unraveled behavior at the elementary level of single input units—the visual sensation generated by stimulating individual long (L), middle (M), and short (S) wavelength–sensitive cones with light. Spectrally identified cones near the fovea of human observers were targeted with small spots of light, and the type, proportion, and repeatability of the elicited sensations were recorded. Two distinct populations of cones were observed: a smaller group predominantly associated with signaling chromatic sensations and a second, more numerous population linked to achromatic percepts. Red and green sensations were mainly driven by L- and M-cones, respectively, although both cone types elicited achromatic percepts. Sensations generated by cones were rarely stochastic; rather, they were consistent over many months and were dominated by one specific perceptual category. Cones lying in the midst of a pure spectrally opponent neighborhood, an arrangement purported to be most efficient in producing chromatic signals in downstream neurons, were no more likely to signal chromatic percepts. Overall, the results are consistent with the idea that the nervous system encodes high-resolution achromatic information and lower-resolution color signals in separate pathways that emerge as early as the first synapse. The lower proportion of cones eliciting color sensations may reflect a lack of evolutionary pressure for the chromatic system to be as fine-grained as the high-acuity achromatic system.

Circuitry to explain how the relative number of L and M cones shapes color experience

The wavelength of light that appears unique yellow is surprisingly consistent across people even though the ratio of middle (M) to long (L) wavelength sensitive cones is strikingly variable. This observation has been explained by normalization to the mean spectral distribution of our shared environment. Our purpose was to reconcile the nearly perfect alignment of everyones unique yellow through a normalization process with the striking variability in unique green, which varies by as much as 60 nm between individuals. The spectral location of unique green was measured in a group of volunteers whose cone ratios were estimated with a technique that combined genetics and flicker photometric electroretinograms. In contrast to unique yellow, unique green was highly dependent upon relative cone numerosity. We hypothesized that the difference in neural architecture of the blue-yellow and red-green opponent systems in the presence of a normalization process creates the surprising dependence of unique green on cone ratio. We then compared the predictions of different theories of color vision processing that incorporate L and M cone ratio and a normalization process. The results of this analysis reveal that—contrary to prevailing notions--postretinal contributions may not be required to explain the phenomena of unique hues.

The spectral identity of foveal cones is preserved in hue perception

Organisms are faced with the challenge of making inferences about the physical world from incomplete incoming sensory information. One strategy to combat ambiguity in this process is to combine new information with prior experiences. We investigated the strategy of combining these information sources in color vision. Single cones in human subjects were stimulated and the associated percepts were recorded. Subjects rated each flash for brightness, hue and saturation. Brightness ratings were proportional to stimulus intensity. Saturation was independent of intensity, but varied between cones. Hue, in contrast, was assigned in a stereotyped manner that was predicted by cone type. These experiments revealed that long (L) and middle (M) wavelength sensitive cones produce sensations that can be reliably distinguished on the basis of hue, but not saturation or brightness. Together, our observations support the notion that color mechanisms near the fovea contain sufficient spatial resolution to produce hue sensations in accordance with each cone’s spectral type.

Sensations from a single M-cone depend on the activity of surrounding S-cones

Color vision requires the activity of cone photoreceptors to be compared in post-receptoral circuitry. Decades of psychophysical measurements have quantified the nature of these comparative interactions on a coarse scale. How such findings generalize to a cellular scale remains unclear. To answer that question, we quantified the influence of surrounding light on the appearance of spots targeted to individual cones. The eye’s aberrations were corrected with adaptive optics and retinal position was precisely tracked in real-time to compensate for natural movement. Subjects reported the color appearance of each spot. A majority of L-and M-cones consistently gave rise to the sensation of white, while a smaller group repeatedly elicited hue sensations. When blue sensations were reported they were more likely mediated by M- than L-cones. Blue sensations were elicited from M-cones against a short-wavelength light that preferentially elevated the quantal catch in surrounding S-cones, while stimulation of the same cones against a white background elicited green sensations. In one of two subjects, proximity to S-cones increased the probability of blue reports when M-cones were probed. We propose that M-cone increments excited both green and blue opponent pathways, but the relative activity of neighboring cones favored one pathway over the other.