Ординатура / Офтальмология / Английские материалы / Seeing_De Valois_2000

144 Karen K. De Valois and Russell L. De Valois

Within the foveal region, the RF center of each midget ganglion cell receives input from just a single L or M cone, with input into the surround from the other cone type (Wässle, Grünert, Martin, & Boycott, 1994). There are thus four subtypes

of L/M opponent cells: Lc Ms, Lc Ms, Mc Ls and Mc Ls. To understand the functional role of these cells, note that these four subtypes fall into two

di erent combinations of pairs, on the basis of similarity of the polarity of the L and M inputs (whether L M or M L), or the polarity of RF center and surround (whether or center). Two of these subtypes ( Lc Ms and Mc Ls) areL M, with excitatory input from L cones and inhibitory input from M cones in the RF as a whole; and two ( Mc Ls and Lc Ms) are M L. Two of the subtypes ( Lc Ms and Mc Ls) are c s, with excitatory center input and inhibitory surround input; and two ( Lc Ms and Mc Ls) are c s. It is not certain whether RF surrounds are cone-type specific, as suggested above, or made up of a combination of L and M cone inputs (De Valois & De Valois, 1993; Reid & Shapley, 1992). It makes surprisingly little di erence which is the case. Since the center mechanism is much stronger than the surround, the presence in the surround of some of the center-type cones would merely slightly diminish the e ective strength of the center.

Outside the foveal region, each midget bipolar still picks up from only one cone, but the midget ganglion cells receive input from more than one midget bipolar (Wässle et al., 1994). It is not known to what extent a given midget ganglion cell in this region picks up just from L-center bipolars, or just from M-center bipolars. Overall, the output of some 4,000,000 cones must feed into some 800,000 midget ganglion cells, so considerable convergence must be present in the retinal periphery. Finally, in the far periphery of the eye, there is no anatomical indication of specificity of connectivity to the bipolar cells; rather, a bipolar cell appears to connect to all the neighboring cones in a small region (Wässle et al., 1994); it would thus have a combination of L and M cones in both RF center and surround. It thus appears likely that there is a loss in cone-type opponency with increasing retinal eccentricity, but the opponency between di erent locations should be maintained. The peripheral Pc cells thus start to resemble Mc cells in their spectral properties. However, at all eccentricities, Mc cells have considerably larger RFs than Pc cells at the corresponding eccentricity (Rodieck, Binmoeller, & Dineen, 1985).

c. Di erence of S and LM Cone Outputs

The pathway from S cones to S-bipolar cells and to S-ganglion cells computes the di erence between the absorption of the S cones and the sum of the absorptions of L and M cones. The “center” and “surround” mechanisms are about the same size, but the center is stronger. As a result, these cells have only spectral opponency with no spatial opponency. In contrast to the paths discussed previously that signal the sum and di erence of the L and M cone responses, the S-cone pathway is very unbalanced. There are many more Sc (L M)s cells than there are Sc (L M)s (de Monasterio, 1979; Derrington et al., 1984; Valberg, Lee, & Tidwell, 1986). In

fact, by some accounts the latter do not even exist (Malpeli & Schiller, 1978). Also in contrast to the L/M path, the S-cone bipolars and ganglion cells appear to maintain their specificity, picking up in their RF centers just from S cones, all the way to the retinal periphery (Kouyama & Marshak, 1992). The S-ganglion cells appear to feed into the Kc layers of the LGN (Hendry & Yoshioka, 1994; Martin, White, Goodchild, Wilder, & Sefton, 1997), and from there to layer IIIB in the cytoxblob regions (see later discussion of cytox blobs) of the striate cortex (Ding & Casagrande, 1997).

3. Summary of Connectivity

There are three main types of retinal processing and three main paths to the cortex, the Mc, Pc, and Kc paths. None of the cells in these three paths signals the amount of light in its region of the retina; rather, they signal the di erences between di erent distributions of light within their RFs. None of the cells in these three paths signals the outputs of just one cone type, either; instead, they signal the sums of or the di erences between the activity of di erent cone types. The cells in the Mc path, in a spatially opponent organization, signal changes in the amount of light absorbed by a small group of L and M cones relative to the amount absorbed by the L and M cones in a larger, overlapping area. Their responses would correspond to the vertical, luminance axis in MBDKL color space (shown in Figure 3). The cells in the Kc path, in a spectrally opponent organization, signal changes in the amount of light stimulating one or more S cones relative to the amount stimulating the neighboring L and M cones. Their outputs correspond to the S or tritan axis in MBDKL space; see Figure 5. Finally, cells in the Pc path (about 80% of the total) have both a spatially and a spectrally opponent organization, at least in the central retina. They signal the di erence between the activity of L and M cones in a small region, in a spectrally opponent organization; but they also signal the changes in the amount of activation of one cone relative to that in the surrounding cones, in a spatially opponent organization. Thus, the cells in the predominant channel from the eye to the cortex, the Pc cells, carry both color and intensity information. In response to full- field or very low spatial frequency stimuli, their outputs would constitute the LM axis in MBDKL color space; see Figure 5. In response to high spatial frequency stimuli, their outputs would contribute to the luminance axis in MBDKL color space.

C. Cortex

1. Striate Cortex

The three main retino-cortical paths have separate projections to the striate cortex (V1), as described above, but within the cortex the paths are no longer discrete. Rather, striate cortex cells combine the outputs of the di erent cell types in various ways. Most of the cortical processing involves building RFs to detect various spatial characteristics (e.g., spatial frequency, orientation, depth) of the pattern

146 Karen K. De Valois and Russell L. De Valois

Responses of a sample of each of the various types of macaque lateral geniculate nucleus (LGN) opponent cells to stimuli that consist of a shift from a white background to various isoluminant stimuli arranged in a circle in MBDKL space. L, M, and S refer to the long, medium, and short wavelength sensitive cones, respectively.The (LM) opponent cells give their peak responses to 0 or 180 , and the S-opponent cells to 90 . The contrasts of these stimuli were chosen to produce sinusoidal variations in absorption by each of the cone types. It can be seen from the sinusoidal fits to the data (with error bars of / 1 SEM) that the processing up to the LGN is very linear.

within a local cortical region (see Geisler & Albrecht, chapter 3, this volume). With respect to color vision per se, the primary processing involves separating color and luminance information, and constructing cells whose color selectivity corresponds to perceptual color appearance.

Figure 6 shows a cortical organization proposed by De Valois and De Valois (1993) that would separate color and luminance information and also construct cells whose chromatic selectivities correspond to the way in which normal human observers under neutral adaptation divide the spectrum into the primary colors of red, yellow, green, and blue. There are two main features to this proposed organi-

Combined with input from a So ( Sc LMs) cell, this would produce a striate cell that fires to white and inhibits to black, but responds poorly if at all to pure color variations, as diagrammed in the top row of Figure 6. Similarly, as shown in the second row of Figure 6, a striate cortex cell (Figure 7b) that sums Lo, Mo, and So cells fires to black and inhibits to white because it has a c s luminance RF. It would, however, be unresponsive to pure color variations, because the color RFs are opposite and thus would cancel.

Cortical cells receiving input from Lo ( Lc Ms) and Mo ( Mc Ls) cells, or from Mo and Lo cells, would respond well to color but not luminance variations, since their color responses would add while their opposite luminance RFs would cancel. This organization by itself would produce L-M color cells that would fire to warm colors (red and yellow) and inhibit to cool colors (blue and green), and M-L cells that fire to cool colors and inhibit to warm colors, respectively. As shown in Figure 6, the further addition of So or So cells would split these into separate red and yellow, and separate blue and green systems, respectively. Examples of these are shown in Figure 8.

If the inputs to cortical cells as diagrammed were perfectly balanced (e.g., if the weights to the Lo and Mo inputs to the cells shown in Figure 8 were precisely equal and thus completely canceled the chromatic components of their responses), this cortical organization would produce cells of six distinct classes, corresponding to the orthogonal axes in the perceptual color space shown in Figure 1. However, the weights of the various LGN-cell inputs are not always balanced, with the result that striate cortex cells are tuned to a variety of color axes, and many respond to both color and luminance patterns to variable extents (Thorell, De Valois, & Albrecht, 1984; Lennie, Krauskopf, & Sclar, 1990). Many functions are carried out in the striate cortex, and surely only a minority of the cells are actually involved in the processing of color. It is clear that certain cells in the striate cortex (cells not present at earlier levels) that respond just to color and are tuned to the perceptual color axes, and others that respond just to white or to black. It is possible, but by no means certain, that only these few cells contribute to our perceptual color organization, with the other cells merely using color as well as intensity information to compute various aspects of the spatial and temporal properties of visual stimuli.

2. Color beyond the Striate Cortex

Early reports (Zeki, 1973) stated that a prestriate region (termed area V4) was specialized for color, all of the cells being color-selective and apparently involved in color processing. It appears, however, that V4 is the major path to the temporal lobe, which is involved in all aspects of form vision, and that no larger a proportion of V4 cells than striate cortex cells are color-selective (Schien, Marrocco, & de Monasterio, 1982). Furthermore, lesions to V4 in monkeys produces only a slight impairment in color discrimination (Schiller, 1993). However, many clinical studies have identified a syndrome of cerebral achromatopsia in humans, a loss of color vision resulting from a prestriate cerebral lesion (Meadows, 1974). Such patients see the

world just in shades of grey (only on one side of the field in the case of those with unilateral lesions). Imaging studies (Tootell, Hadjikhani, Liu, & Cavanagh, 1998) have identified a critical color region in human subjects anterior to the striate cortex, in a region that appears not to be homologous with monkey V4. It is thus possible that in humans, but not in monkeys, a prestriate region is critical for color perception.

It is not clear what transformations of color information per se take place past the striate cortex, although one likely possibility is that of interactions with surrounding regions to enhance color constancy. The visual system must compensate for the changing color of the illumination in the course of the day, from yellowish at dawn and dusk to bluish at noon on a clear day, in order to correctly identify the color of objects. Most of this compensation takes place at the level of the receptors, in the adaptation processes described above. However, longer distance interactions are involved as well, as seen in the familiar demonstrations of color contrast, in which, for instance, a red surround makes a central patch of gray appear greenish. The processing up and through the striate cortex is local, and such color-con- trast e ects are not seen at these levels (De Valois, Snodderly,Yund, & Hepler, 1977). Grouping together cells of similar selectivities in di erent prestriate areas (e.g., to motion or color) would allow interactions over longer distances. Such appears to be the case in prestriate area V4, where long-distance color contrast e ects are found: the responses of cells to chromatic patterns in the centers of their RFs are modified by the color of the surround (Schein & Desimone, 1990).

III. CHROMATIC DISCRIMINATIONS AND THEIR

PHYSIOLOGICAL BASES

A. Chromatic Discrimination of Uniform Stimuli

Many studies over the years have measured the basic chromatic capabilities of human observers for lights presented as large homogeneous or bipartite fields (2 or more in diameter). These experiments examine just chromatic discriminations, largely ignoring the spatial characteristics of the stimuli.

1. Wavelength Discrimination

A wavelength discrimination experiment determines the smallest di erence in wavelength between two monochromatic lights (e.g., in a bipartite field) that an

FIGURE 8 The receptive fields (RFs) for cone-specific stimuli for three cortical cells that receive spectrally opponent LGN inputs. Note that each of these cells combines inputs from all the LGN opponent cell types. The cell at top combines Lo, Mo and So and would thus respond preferentially to red, with little response to luminance variations, since the L and M receptive field centers for luminance are in opposite directions. The cell in the middle has just the opposite organization, Lo, Mo, andSo, and would thus respond to green. The cell at bottom has inputs of Lo, Mo, and So and would thus respond best to yellow. (Data collected with N. P. Cottaris, S. D. Elfar, and L. E. Mahon.)

152 Karen K. De Valois and Russell L. De Valois

observer can discriminate, examining this for lights in di erent parts of the spectrum. The observer usually has control of both the wavelength and the intensity of the test field. She or he is instructed to change the wavelength until the standard and test stimuli are just discriminably di erent, then to try to eliminate the perceived di erence by adjusting the intensity of the test light. The latter step is necessary to ensure that the discrimination is based upon a wavelength di erence rather than a change in e ective intensity.The absolute values obtained depend upon adaptation level, field size, and retinal eccentricity, among other things. The function obtained for wavelength discrimination in the fovea at phototopic light levels is roughly W-shaped. The minimal discriminable wavelength change, , passes through two shallow minima—at about 490 and 590 nm, respectively—where a change in wavelength of 1 nm can reliably be detected under optimal conditions (Wright & Pitt, 1934, and many others). Making the field smaller, moving it into the retinal periphery, or reducing the mean light level will all increase the measured thresholds, though not necessarily uniformly. Lowering the luminance level, for example, will tend to increase more at the spectral extremes than for midspectral lights (Bedford & Wyszecki, 1958).

It is clear that hue discrimination in general is primarily limited by the characteristics of the receptor photopigments and by the processing that takes place in the retino-geniculate path. The visual stimulus contains much more information than we can perceive and discriminate, and it appears that almost all of this loss occurs early in the path, due to the presence of a very limited number of receptor types and of only three paths from each region of the retina to the cortex. There appears to be little additional loss once the information reaches the cortex, presumably re- flecting the fact that there are an e ectively unlimited number of cells to process color information at that level.

The normal human wavelength discrimination curve, showing two spectral regions of best discrimination, reflects the characteristics of the cone photopigments and the presence of just two opponent-cell types in the retina and LGN. The region of good discrimination in the long wavelengths at about 570 nm is where the rate of change in the L minus M (or M minus L) signal is highest, and where the LM opponent cells show the largest change in firing with a change in wavelength (De Valois, Jacobs, & Abramov, 1964). The second region of good discrimination, at short wavelengths in the region of 490 nm, is attributable to the fact that the S-LM opponent cells show the best wavelength discrimination in this region (De Valois et al., 1964), where the slope of the S-cone pigment curve di ers most from that of the combined L and M cones.

This explanation of the two regions of best discrimination in the wavelength discrimination function of normal observers is supported by data from dichromats (see discussion of color defects below).These color-defective observers, missing one of the cone types, and thus necessarily one of the opponent cell types, each show only one region of good color discrimination, at only short wavelengths for those missing L or M cones, and at only long wavelengths for those missing S cones.

2. Purity Discrimination

When a white light is added to a monochromatic light, the excitation purity of the monochromatic light is reduced. Excitation purity is defined (in the CIE chromaticity diagram, see Figure 2) as the ratio between the distance from the white point to the test point and the distance from the white point to the corresponding point on the spectral locus. Reducing excitation purity corresponds perceptually to a reduction in a light’s saturation (see Figure 1). The ability to discriminate changes in purity is determined most commonly by measuring the purity change required to produce the first discriminable step from white towards various spectral loci (i.e., how much monochromatic light has to be added to white for it to be seen as colored). Other measures are the number of discriminable steps in purity between the monochromatic point and white, or the size of the first discriminable step from monochromatic light towards white. With a photopic, foveal stimulus, the purity (or saturation) discrimination function shows a sharp minimum at about 570 nm, a spectral locus seen as a slightly greenish yellow by a normal observer under neutral adaptation (Priest & Brickwedde, 1938; Wright & Pitt, 1937). In this region of the spectrum, a large amount of monochromatic light must be added to white in order for a subject to detect a change. The function rises sharply (implying better discrimination) in the long wavelengths and somewhat less precipitously in the shorter wavelengths. Both spectral extremes appear very highly saturated, very different from white.

Since spectrally opponent LGN cells clearly carry chromatic information to the brain, and spectrally nonopponent cells carry achromatic information, one would expect that the relative saturation of various spectral regions would be proportional to the relative sensitivities of these di erent cells types to lights of di erent wavelengths. The ratio of opponent to nonopponent LGN cell responses to various isoluminant monochromatic lights (De Valois et al., 1966) shows close agreement with the human purity-discrimination function. The minimum saturation of lights in the region of 570 nm is accounted for by the fact that this spectral region is that to which the nonopponent cells are most responsive, and is the region to which the LM opponent cells are the least responsive, since both the L-M and the M-L opponent are crossing over from excitation to inhibition in this region, leaving only the relatively few S-opponent cells responding here.The spectral extremes, on the other hand, produce little output from the nonopponent cells, but large responses from the opponent cells and are thus very saturated. Direct tests of the responses of various opponent cell types to monochromatic lights of di erent purities (De Valois & Marrocco, 1973; Valberg, Lee, & Tryti, 1987) confirms this conclusion.

3. Intensity, Luminance, and Brightness

A spot of light has a certain chromatic component related to its hue and saturation, but it also has an intensive component.To measure the intensive dimension of lights of various wavelengths, one must somehow eliminate the contribution from purely