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

Abstract

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 everyone's 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.

An S-cone circuit for edge detection in the primate retina

“…They can detect edges based either on luminance or spectral contrast but are unlikely to have any role in hue perception. Moreover, the S vs. L+M spectral tuning in both neurons does not match the cone inputs to blue-yellow hue perception 23,64,68,78,79 and a subset of midget RGCs with cone inputs matching the fundamental hues 21,22,27,70 has been proposed to mediate hue perception instead (for review, see Neitz & Neitz 54 ). These L vs. M midget RGCs with significant S-cone input to the surround receptive field are another controversial midget RGC subtype that warrants additional investigation.…”

Evolution of the circuitry for conscious color vision in primates

“…The combinations of S-cone inputs to L/M opponent midget ganglion cells produces exactly the hue axes corresponding to phenomenological hues. 62,63 As evidence, for the proposed hue encoding midget ganglion cells, a small number of L/M opponent ganglion cells with S-cone input have consistently been reported at different levels of the visual pathway, in the retina, 66,67 LGN 69,70 primary visual cortex 71,72 and at higher centers in the ventral visual processing stream, in inferior temporal cortex. 73 In our own laboratory, recording from an ex vivo preparation of macaque retina 6,74 we have confirmed the presence of a small subset of L/M opponent midget ganglion cells with S-cone input.…”

“…For the submosaics of midget bipolar cells with GABA-mediated S-cone feedforward input, these four types have cone inputs, as discussed below, that correspond exactly to those responsible for the four unique hues in modern humans. 62,63 L-ON-center for yellow, L-OFF-center for blue, M-ON-center for green, and M-OFF-center for red. In each case, the center L or M cone has an opposed feedforward input from an S-cone.…”

“…DeValois and DeValois 65 have, for example, outlined a specific model for how this could be done. Alternatively, other vision scientists including ourselves 59,62,[78][79][80][81] have pointed out that if there is a population of ganglion cells specifically dedicated to color, elaborate anatomical circuits to separate luminance from color signals from the midget ganglion cells are rendered unnecessary. Indeed, this appears to be the case and the system presented here is a beautiful example of efficient coding in the nervous system.…”

“…However, each is tuned through visual experience by a normalization process to be insensitive to the average spectral distribution from the environment-the colors we call white (or gray). 62,[82][83][84] Since, they are encoding spectral contrast across a boundary, each one evolved as a 'spectral reflectance' detector. M-(S+L) cells are detectors of surfaces (which we call 'green') that reflect more middle-wavelength light compared with the average spectrum.…”