Mapping color perception to a physiological substrate

Linking Color Opponency with Cone Antagonism

We are able to perceive an amazingly diverse range of hue, or what we call in the vernacular color. The tremendous variability in the spectral composition of light reflected from surfaces lends itself to eliciting a daunting gamut of more than 100,000 discriminable colors, and the variation in the names we assign these colors is limited only by the scope of human experience. Yet, even with this variation, no demographic culture requires more than 11 color names to describe the quality of any hue (reviewed in Boynton, 1975). Of these 11, 5 can be described using either black or white in combination with the four unique hues—blue, green, yellow, and red (Bornstein, 1973). These four hues are themselves irreducible as percepts, and in that sense, each can be mapped at least conceptually to a perceptual channel whose activity correlates with that hue. The combined activity between channels presumably is what produces the rich variety of colors we experience.

The precise design of our visual system rigidly constrains how the activity of the color channels is mapped to hue sensation. Our ability to discriminate surfaces based on differences in spectral reflectance alone arises from a neural comparison of the rates of quantal absorption by the S-, M-, and L-cone photoreceptors (see Lennie and D'Zmura, 1988, for review). This neural comparison delimits color activity in the brain and has a characteristic signature that imposes upon hue perception a natural constraint. The four unique hues are organized into mutually exclusive or opponent pairs, blue/yellow (B/Y) and red/green (R/G). The members in each pair are opponent in the sense that we cannot perceive them simultaneously; their perceptive fields are spatially coextensive and cancellatory. We may perceive hue combinations between these pairs—for example, red and blue yielding a percept that is at once both (namely, violet)—but not combinations within a pair. Thus, there are no such hues as red-green or blue-yellow; we do not experience these percepts and therefore do not have names for them. This inherent phenomenology is explained in abstract terms by identifying each opponent pair with an independent color channel, B/Y and R/G, and through these channels all color perception is mediated.

A diverse body of psychophysical data implies that the B/Y and R/G channels each correlate with a neural pathway in which signals from the three cone types converge with one another in different antagonistic combinations (Hurvich and Jameson, 1957). The particular combination of cone antagonism bestows upon each channel a unique spectral sensitivity that correlates strongly with our perception of hue across the visible spectrum. For B/Y opponency, signals from S cones are combined antagonistically with an additive signal from M and L cones. This combination is abbreviated as S/(M + L), where “/” indicates antagonism or subtraction. Very often the denotation S-(M + L) is used instead, and the psychophysical spectral sensitivity of the channel (which by definition cannot be a negative number) is derived from the absolute value of the difference (Fig. 64.1). For R/G opponency, signals from L cones are combined antagonistically with those from M cones (abbreviated as L/M or L-M; Calkins et al., 1992). There is also a strong input from S cones into the R/G channel with the same polarity as the L-cone signal—the S signal can be canceled with appropriate stimulation of the M cones (Hurvich and Jameson, 1957; Stromeyer et al., 1998). Thus, much of the short-wavelength spectrum appears both blue and red, indicating activation of both the B/Y and R/G channels (DeValois et al., 2000a; Krauskopf et al., 1982; Wooten and Werner, 1979). The denotation “L/M” is a generalization that most visual scientists accept as a reasonable representation of the R/G channel but does not incorporate the S contribution. Each particular combination, S/(M + L) or L/M, therefore represents the minimal condition that describes the defining opponency within a neural pathway consistent with the psychophysical properties of the appropriate color channel.

Figure 64.1..  

A two-stage cone-antagonistic model of color opponency. For B/Y opponency (left), signals from S cones are combined antagonistically (indicated by “−”) with the sum of signals from M and L cones (indicated by “+”); the net spectral sensitivity of the channel is given by the absolute value of the difference of the cone terms. Similarly, for R/G opponency (right), a combined signal from L and S cones is subtracted from signals from M cones. The K coefficients scale the spectral sensitivity of each cone and represent the combined effects for both stages in the model.

There are therefore two primary considerations in assigning an anatomical substrate to the cone-antagonism within the S/(M + L) and L/M pathways: (1) the source of each pure cone signal prior to the site of antagonistic convergence and (2) the mechanism of antagonism itself. The first addresses the mechanism through which excitation from each cone type is collected or pooled and whether this pooling is indeed independent of the other photoreceptors (represented as “Stage 1” in Fig. 64.1). This stage accurately conveys the spectral sensitivity of the cone, including amplitude changes in cone sensitivity due to adaptation, and possibly modulates the cone signal further through its own intrinsic filters. In retinal terms, this stage likely corresponds to one or more types of bipolar cell that collect from cones and feed a glutamatergic excitatory signal forward to the ganglion cells. The second consideration addresses the anatomical site and mechanism through which signals from different cone types converge with opposite polarity, the so-called critical locus of opponency (“Stage 2” in Fig. 64.1; Teller and Pugh, 1983). This stage too could modulate or filter the collected cone signal through its own intrinsic properties. However, unlike the first stage, its output depends not on the spectral sensitivity of one cone type, but on the difference in sensitivity between two or more types. This difference signal forms the spectral signature of the color channel itself (for review, see Calkins and Sterling, 1999). In the primate retina, such antagonism between cones could arise through the convergence of an excitatory signal, say from a bipolar cell, with an inhibitory signal through lateral connections with horizontal cells (GABA-ergic) or amacrine cells (glycinergic), or more likely some combination of these. In the case of B/Y opponency, the antagonism is thought to involve the convergence of strictly excitatory signals from bipolar cells that respond to light with opposite polarity, that is, OFF cells versus ON cells. Thus, cone antagonism is not necessarily synonymous with physiological inhibition.

Characteristics of a Color Pathway

There is great potential for spatial and temporal modulation of each cone's signal through the two stages described in Figure 64.1 (e.g., Pugh and Mollon, 1979), the nature of which is well beyond the scope of this chapter. Because the sensitivity of each cone depends on ambient conditions, there is also the potential for spectral modulation (represented by the coefficients K in Fig. 64.1). In effect, this modulation scales the amplitude of the cone sensitivities relative to one another, depending on the spectral composition and intensity of the ambient illumination. This shift greatly influences the resultant spectral sensitivity of the S/(M + L) and L/M pathways and therefore how the activity of the pathways partitions the visible spectrum into regions of dominant hue (Fig. 64.2). Thus, the color appearance of a monochromatic light under typical psychophysical conditions (i.e., a small spot on a larger adapting field) is directly related to the spectral sensitivity and activity of each channel.

Figure 64.2..  

Data points represent the spectral sensitivity of the R/G (open squares) and the B/Y (filled circles) color channels estimated from chromatic scaling measurements (Romeskie, 1978). Solid curves were calculated from the model in Figure 64.1. The color of each curve represents the chromatic valence at each wavelength. The bottom traces represent the scaled sensitivity of the R/G and B/Y channels under typical psychophysical conditions. The color of the individual peaks represents the hue sensation of a monochromatic light at that wavelength. Threshold detection of monochromatic test lights would be mediated by the most sensitivity mechanism at each wavelength. Lights at and just above threshold elicit unique hues, while lights well above threshold generally fall and are detected through both R/G and B/Y channels. The location of unique yellow corresponds to the neutral point of the R/G channel, where detection is mediated solely by the B/Y channel (arrow). (See color plate 40).

This relationship between spectral sensitivity and hue perception allows some key predictions about the wiring of the S/(M + L) and L/M pathways. Most obviously, the output of a pathway should result in one hue and one hue alone, whose quality depends solely on the cone term dominating that output (as indicated in Fig. 64.2). Therefore the unique hues—blue, green, yellow, and red—ought to correlate closely with the activity of a pathway functioning in isolation. This is all to say that the S/(M + L) and L/M pathways should, in some measure, demonstrate separability and independence. As a corollary to this condition, the neutral points of each pathway (wavelengths where the cone terms cancel) ought to correspond to a locus of unique hue, where the other pathway solely mediates detection. For example, the wavelength at which the L- and M-cone terms in the L/M pathway cancel one another (570 to 580 nm under typical adaptive conditions) corresponds to unique yellow because detection is mediated only by the (M + L) envelope of the S/(M + L) pathway (Fig. 64.2). The chromatic neutral points are therefore closely dependent on the relative shift in cone sensitivity (reflected in the coefficients K in Figs. 64.1 and 64.2) prior to the stage of antagonistic convergence. The neutral points, then, represent the chromatic signature of the S/(M + L) and L/M pathways, and whatever circuitry in the visual system lends itself to establishing the critical locus of cone antagonism should in some measure support this signature.

The optics of the eye, the spatial sampling of retinal neurons, the ratio of rods to cones, and the relative numbers of L and M cones all change dramatically with increasing retinal eccentricity. Despite these variations, for normal trichromatic observers the S/(M + L) and L/M neutral points are remarkably invariant (Hibino, 1992; Kuyk, 1982; Nerger et al., 1995). Along these same lines, when appropriate stimuli are delivered to the peripheral retina, even as far out as 90 degrees, color is perceived with the same range of hues and with the same capacity to discriminate hues as in the fovea (Gordon and Abramov, 1977; Noorlander et al., 1983; Stabell and Stabell, 1982; van Esch et al., 1984). It is true that larger stimuli are required in the peripheral retina to produce comparable sensations, but this is not surprising given the decrease in spatial resolution of retinal mosaics and in the sensitivity of the color channels.

Linking Circuitry with Cone Antagonism

In short, the fundamental features of the color opponent channels are similar between the fovea and the peripheral retina—despite the common and mistaken belief that color discrimination is a special function of the central retina. This consistency suggests two general possibilities for wiring the S/(M + L) and L/M pathways. The first possibility is that cone antagonism is established in the retina, within the presynaptic circuitry of one or more types of ganglion cell. In this case, the spectral signature of the color pathways begins with the particular circuitry producing the cone antagonism and is then conveyed to the cortex in a manner that is conserved across retinal eccentricity. This would place both stages of the generalized model in Figure 64.1 within the retina. The second possibility is that the cone antagonism inherent in color opponency is established later in the visual pathways, for example, in V1. In this instance, one or more types of ganglion cell could carry cone signals from the retina (Stage 1 in Fig. 64.1), and the antagonism (Stage 2) would be established in a central neuron where those signals converge with opposite polarity (e.g., ON-center vs. OFF-center cells). In this scheme, any antagonistic interactions within the ganglion cell receptive field, such as those between center and surround, would be ancillary to the critical spectral antagonism established at the central neuron. Spectral variations within the ganglion cell receptive field across retinal eccentricity (e.g., as the ratio of L to M cones changes) could then be washed out by cortical wiring.

Most visual scientists are willing to accept that color opponency at least begins in the retina for both B/Y and R/G opponency. This inference is supported by the vast physiological literature demonstrating cone antagonism within the receptive fields of many ganglion cells, mainly in those providing input to the parvocellular (P) region of the lateral geniculate nucleus (LGN; for reviews, see references in Table 64.1). This is especially so for the massive subset of these cells serving the central visual field. There, the net spectral sensitivity to full-field stimulation is generally (but not always) cone antagonistic, either S/(M + L) or L/M (Fig. 64.3), although many other combinations also have been found (de Monasterio and Gouras, 1975). The key issue is the circuitry for this antagonism and whether it is sufficient to explain the spectral, spatial, and temporal properties of the opponent channels. Of particular interest for this chapter is whether the retinal circuitry is conserved across eccentricities or whether more central mechanisms are necessary to explain the consistent spectral signature of the opponent channels.

Figure 64.3..  

Top: spectral sensitivity of a nominal R/G opponent ganglion cell that responds with an increase in firing rate to long wavelengths (open squares) and with a decrease to middle and short wavelengths (filled squares). The curve was calculated from the R/G model in Figure 64.1. Bottom: spectral sensitivity of a B/Y opponent ganglion cell that responds with an increase in firing rate to short wavelengths (open circles) and with a decrease to middle and long wavelengths (filled circles). The curve was calculated from the B/Y model in Figure 64.1. (Data replotted from Zrenner, 1983b.)

This chapter will explore two general schemes for wiring cone antagonism in a ganglion cell receptive field (Fig. 64.4). The first is through the simple convergence of signals from cones of different types via strictly excitatory cells that respond to light with opposite polarity, that is, OFF versus ON bipolar cells. This sort of wiring is likely to underlie the S/(M + L) spectral sensitivity of the small bistratified ganglion cell, and this chapter will discuss how the cell might contribute to B/Y opponency (see also Calkins, 2001). The second scheme involves the convergence of excitatory and inhibitory inputs in such a way to render the ganglion cell color opponent. For example, the excitatory center of a foveal P (or midget) ganglion cell is derived from a single cone via a midget bipolar cell, while its inhibitory surround is derived from a combination of cone inputs via GABA-ergic or glycinergic lateral connections (Calkins and Sterling, 1999). This chapter will discuss the mechanism through which the ganglion cell's spectral sensitivity reflects the difference between these signals across retinal eccentricities and the implications for R/G color opponency.

Figure 64.4..  

Two schemes for wiring cone antagonism in the receptive field of retinal ganglion cells. Right: antagonism for the S-ON/(M + L)-OFF ganglion cell (blue) established through converging ON and OFF bipolar cells. Left: antagonism for the midget cell (green) via convergence of excitation from a bipolar cell and inhibition via horizontal (H) and amacrine (A) cells. (See color plate 41.)