Ординатура / Офтальмология / Английские материалы / Seeing_De Valois_2000

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

seen as white under neutral adaptation.This color space has several very useful properties. For example, a mixture of any two lights in any proportions will lie somewhere along the straight line connecting the two mixture components. A normal observer in a state of neutral adaptation will generally see the point labeled A as blue, and the point labeled B as yellow. If the two lights represented by those points are mixed, the chromaticity of the resulting light will lie on the line AB. This line passes through the region most observers see as white under neutral adaptation. Thus, this intuitively unlikely result—that blue and yellow can mix to produce white—can be deduced from inspection of the color space. An excellent discussion of the development and the characteristics of the CIE 1931 xyz chromaticity space is given by Kaiser and Boynton (1997).

3. MBDKL Physiological Color Space

The third color space that we will describe briefly was derived not from color appearance (like the double-cone space) or from color matching (like the CIE 1931 xyz space), but from physiological data. We now have a quite precise knowledge of cone photopigment spectral sensitivity curves (see Figure 4) and of the neural transformations of the cone outputs in the retinal processing (see Figure 5). This color space is based on such data. A cone-based color space was initially developed by MacLeod and Boynton (1979). It was later elaborated, on the basis of di erent chromatic cell types seen in the path through the lateral geniculate nucleus (LGN) to the cortex, into a three-dimensional space by Derrington, Krauskopf, and Lennie (1984). We will refer to it as the MBDKL color space. A version of this is shown in Figure 3. The outputs of the cone photoreceptors, with peak spectral sensitivities in the short (S), medium (M) and longer (L) wavelengths, respectively, are compared at later neural levels by neurons that sum and di erence their outputs (De Valois, 1965; De Valois, Abramov, & Jacobs, 1966; Derrington et al., 1984), as discussed below. The three axes of this color space correspond to the three types of neurons in the retina and LGN that carry the information to the cortex about these sums and di erences. The vertical axis represents luminance (light intensity weighted by the spectral sensitivity function of the visual system, modeled as the sum of 2L M cone outputs). Two orthogonal axes lying in a horizontal plane of the sphere represent the di erence of L and M cone absorptions (the LM axis), and the variation in S-cone absorption, with L and M cone absorptions held constant (the S or tritan axis). In this space, any point can be specified by its azimuth (representing the angle in a horizontal plane, with the LM axis defining the 0 –180 directions, and the S-varying axis defining the 90 –270 directions) and its elevation, where the elevation represents luminance with respect to the midpoint. Within any horizontal plane, all points represent stimuli that are equated for luminance (thus, an isoluminant plane), with di erent horizontal planes representing di erent luminance levels.

Below we shall briefly discuss first the anatomy and physiology underlying color

FIGURE 3 The MBDKL physiologically based color space in which the vertical axis represents luminance (defined as the sum of long [L] and medium [M] cone outputs), and the two spectrally opponent axes seen at an early neural level are orthogonally represented on the horizontal plane. All points that lie on a common horizontal plane represent isoluminant stimuli; hue varies with angle around the horizontal plane; saturation increases along any radius in a given horizontal plane. The point L-M is by convention defined as 0 ; S is 90 ; M-L is 180 ; and S is 270 .

vision, including the photopigments and their spectral sensitivities, the distribution of di erent receptor types across the retina, receptor function, types of retinal computations, and color processing in the cortex. Then we shall discuss several behavioral (or psychophysical) aspects of color vision, including chromatic opponency, perceptual dimensions of color, chromatic discriminations, spatial and temporal contrast sensitivity, color appearance, and color motion. In each case, we shall attempt to relate the behavioral aspects of color vision to the underlying physiology.

II. PHYSIOLOGY

A. Photopigments and Spectral Sensitivity

The initial stage in the visual response is the absorption of light by the photopigments in the receptors. The cones are the most relevant receptors for color vision, indeed for all vision at high light levels. The absorption of light by a cone photopigment triggers a complex series of reactions, leading ultimately to synaptic transmission at the cone pedicle. Here we discuss briefly some characteristics of the photopigments that are relevant in determining whether a given photon will be absorbed when it encounters a photopigment molecule.

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The receptor outer segment is filled with about 500–1000 disks, each containing millions of photopigment molecules.The photopigments in our rods (the receptors used for vision at low light levels) and in all the di erent types of cones are built on a very similar plan: a chromophore, retinal (Vitamin A aldehyde) is attached to a large protein molecule called an opsin. Such photosensitive pigments (called rhodopsin in rods) are found in the eyes of all animals and have been highly conserved in the course of evolution, having arisen a billion or more years ago in bacteria. Rhodopsin and the similar cone opsins are uniquely useful for vision for two reasons. One is that the capture of just one photon is su cient to break the molecule apart into its separate retinal and opsin components, so it has attained ultimate photosensitivity. The other reason is that when the retinal breaks away from the opsin, it reveals an enzymatic site. The opsin now acts as an enzyme to initiate a cascade of chemical reactions, providing the amplification of the tiny energy of a few photons to the much larger energy required to activate neurons and transmit information through the nervous system. Although the cone transduction sequence has not been as exhaustively studied as that in rods, there are good reasons to assume that it is similar.

The basic shape of the spectral sensitivity curve of rhodopsin and the various cone opsins is determined by retinal, which is common to all receptor photopigments. All receptors therefore have similarly shaped spectral sensitivity curves. But the spectral region to which the molecule is most sensitive is also a ected by parts of the opsin in the vicinity of the retinal attachment site, and each di erent receptor type, rods and three (or more) cone types, has a somewhat di erent opsin. The substitution of one amino acid for another at a particular point in the opsin molecule can shift the spectral sensitivity curve to longer or to shorter wavelengths. Amino acid substitutions that produce major shifts in spectral sensitivity have created three primary regions of receptor peak sensitivities (Schnapf, Kraft, & Baylor, 1987; Schnapf, Kraft, Nunn & Baylor, 1988) (see Figure 4). These are found in the S cones (with greatest sensitivity at about 430 nm), in rods (which peak at about 500 nm), and in L and M cones (with peaks ranging from about 530 to 565 nm). Amino acid substitutions in L and M opsins that produce smaller spectral shifts have created a variety of L and M photopigment types among the normal and colordefective human population (Neitz, Neitz, & Jacobs, 1991). For example, there are M cones with peak absorption at 530 and others at 535 nm, and L cones with peak sensitivities at 555 or 560 or 565 nm.

All humans appear to have the same S-cone and rod photopigments, but they di er somewhat in their L and M cone pigments. About 8% of human males and about 1% of females have color vision deficiencies, most of which are the so-called red–green deficiencies.The prevalence of this particular type of color-vision defect can be accounted for by the chromosomal location of the various photopigment genes. The rod photopigment gene is on chromosome 3; the S cone pigment gene is on chromosome 7; and both the M and the L cone photopigment genes are side-

FIGURE 4 Three representative cone pigments in primates, based on the report of Baylor, Nunn, and Schnapf, 1987. (S, short; M, medium; L, long).

by-side on the X chromosome (Nathans, Thomas, & Hogness, 1986). Because they are adjacent to one another on the same chromosome, the L and M photopigment genes are subject to interchanging parts in the process of crossing over during meiosis, resulting in a variety of L and M gene types (alleles) in the population. The extreme case is one in which the two genes end up being identical, thus specifying only one longer wavelength (either M or L) photopigment. Because males only inherit one copy of the X chromosome, whereas females inherit two, a female would have to inherit defective genes from both parents (but a male only from his mother) to be color-defective. An interesting corollary of this is that many females appear to have more than just two LM pigments, and thus more than three di erent cone types (Neitz & Jacobs, 1990), but females with more than three cone types nonetheless have only a trichromatic color vision system (Nagy, MacLeod, Heyneman, & Eisner, 1981). Presumably, the two L cones that such a woman might possess are treated as being identical by the retinal organization and thus do not lead to an additional chromatic dimensionality. This strongly suggests that the trichromatic limit to human color vision is the result of only three types of analyses in the retina, and/or of only three paths from the retina to the cortex, not, as was long supposed, because of the presence of only three cone types.

other. This polarization change in the outer segment is conducted to the synaptic region, where it produces a change in the rate of synaptic chemical release. A decrement in light absorbed shifts the balance towards depolarization and leads to an increase in synaptic transmitter release to activate the next neurons in the chain to the brain; an increment in light absorption shifts the balance towards hyperpolarization and produces a decrease in transmitter release. As we move our eyes around in a scene, as we do constantly, the amount of light absorbed by each receptor oscillates up and down, as the intensity or the wavelength of light being absorbed varies. The receptors faithfully transduce these oscillating increases and decreases in light absorption into oscillating amounts of synaptic transmitter release.

The receptor outer segment membrane is maintained at a certain level of polarization (roughly 40 mV) by a balance between the action of cGMP, which opens pores in the cell membrane allowing Na and Ca ions to enter and depolarize the cell, and a metabolic pump that expels these ions and hyperpolarizes the cell. The polarization varies as the level of cGMP varies, and that in turn is determined, moment by moment, by the changes in absorption of light in the outer segment disks. cGMP is constantly being produced, but it is broken down by phosphodiesterase, which in turn is produced by a chemical, transducin, activated by the breakdown of rhodopsin or the cone opsin by light. With a decrease in light being absorbed by the receptor, less phosphodiesterase will be produced, the level of cGMP will go up, the membrane will be depolarized, and the receptor will secrete transmitter chemicals to the next neurons in the chain. An increase in light being absorbed by the receptor will produce more phosphodiesterase, the level of cGMP will go down, and the membrane will be hyperpolarized, resulting in a decrease in the amount of receptor transmitter chemical being released.

A second set of reactions also plays an important role in the responses of receptors. As cGMP opens membrane pores, Ca ions flow in and inhibit, with a brief time delay, the production of cGMP; conversely, when the pores are closed, the internal Ca level falls and the production of cGMP increases.This negative feedback has the e ect of making the receptor responsive to transient increments and decrements but less so to the steady-state illumination level. It thus forms the second stage, after the variations in pupil size, in the process by which the visual system minimizes responses to the illuminant in order to concentrate on capturing information about visual objects.

B. Retino-Geniculate Processing

1. Retinal Connectivity

There are two levels of synaptic interaction in the retina: among receptors, bipolar cells, and horizontal cells in the outer plexiform layer, and among bipolar cells, amacrine cells and ganglion cells in the inner plexiform layer. The path from receptors to bipolar cells to ganglion cells leads towards the brain; horizontal and amacrine

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cells form lateral connections and provide for data processing within their respective plexiform layers.

Anatomists have identified many di erent subtypes of each of the various neural elements in the retina, for example, as many as 25 di erent varieties of amacrine cells. However, the function of many of these subtypes, and indeed whether or not some of the slight anatomical di erences have any functional significance at all, is unknown. What we present here is a simplified version of the anatomical arrangement, based on the currently well understood cell types and connections, including only those clearly relevant to color vision.

It is equally important for the visual system to detect increments and decrements in light intensity, and to detect changes in wavelength toward longer and toward shorter wavelengths. Receptors presumably depolarize and hyperpolarize symmetrically about the mean depolarization level, and can thus signal changes in these opposite directions equally well.When the form of the information is changed from variations in graded potentials of receptors and bipolar cells to variations in spike firing rate at the level of ganglion cell axons (a transformation that is needed to transfer the information the long distance to the thalamus and from there to the cortex), this symmetry is lost. Cells can fire bursts of spikes at rates up to about 400/ sec, but rapid firing rates are very expensive metabolically. For a single cell to carry information equally well about increments and decrements from the mean adaptation level, it would have to fire an average of 200 spikes/sec, day and night. The visual system has instead divided the task between two cells in each location, each with a low maintained rate (of perhaps 10 spikes/sec), with one responding from 10 to 400 spikes/sec to various sizes of increments in absorption, and the other responding from 10 to 400 spikes/sec to decrements in absorption. This division of labor takes place at di erent levels, and with di erent organizations, for rods as compared to L and M cones, and seemingly almost not at all for S cones.

Receptors contact bipolar and horizontal cells with two di erent sorts of connections.The receptor synaptic region has a number of pouches, and receptors contact bipolar and horizontal cell processes that invaginate the pouches. All receptors, rods and all types of cones, make this sort of connection. In addition, L and M cones make synaptic contact with a di erent class of bipolars outside the pouches, on the basal parts of the synaptic region (Missotten, 1965). The important fact is that invaginating and basal bipolars respond in opposite ways to the receptor transmitter, and thus in opposite ways to increments and decrements in the amount of light absorbed by the receptor (Famiglietti & Kolb, 1976). Receptors depolarize, and thus increase synaptic transmitter release, in response to decrements in light absorption. The basal bipolars are depolarized by the receptor transmitter and thus also depolarize to decrements. Invaginating bipolars, however, invert the receptor signal and thus depolarize to increments in light absorption.

Two di erent types of bipolar cells, midget and di use bipolars, pick up from L and M cones, and each of these is one of a pair, with one making invaginating contacts and one making basal contacts (Kolb, Boycott, & Dowling, 1969; Mariani,

1981). Each L and M cone, therefore, feeds into at least four di erent bipolars, two of which depolarize to increments and two to decrements. The L and M cones thus have separate, symmetrical systems for responding to increments and decrements starting at the bipolar level. This separate, symmetrical arrangement is continued up to the cortex.The midget bipolars contact midget ganglion cells, which in turn project up to the parvocellular (Pc) layers of the LGN. The di use bipolars contact parasol ganglion cells, which project to the magnocellular (Mc) layers of the LGN. Within each of these midget-Pc and parasol-Mc systems, there are separate cells responding primarily to increments and decrements in light.

The circuitry for S cones and for rods, however, is quite di erent. S cones contact a special type of invaginating bipolar (Mariani, 1984), which has no basal mate (there are some reports of certain di erent types of bipolars making basal contacts with S cones, but the circuitry involved is not known). The S-bipolar in turn contacts a di erent ganglion cell from those contacted by L and M cones, a bistratified ganglion cell that depolarizes to S-cone increments (Dacey & Lee, 1994). These S- ganglion cells appear to project to the koniocellular (Kc) layers of the LGN. The S- cone system is thus unbalanced, with ganglion cells and LGN cells that fire to S- cone increments, but few if any that respond to S-cone decrements.

Rods have still a third type of retinal organization and projection pattern to central levels. Rods do not have a separate path to the brain, but rather feed up through the same paths as the L and M cones. Although there is only an invaginating rod bipolar (which, like other invaginating bipolars, responds to light increments), the rods generate symmetrical incremental and decremental systems at a later level, through an intermediate type of rod amacrine cell. The rod bipolars contact rod amacrine cells, which in turn contact di use and midget ganglion cells. The rod amacrine cells each make two di erent types of connections, one a direct excitatory contact with an incremental ganglion cell, and a second sign-inverting connection with a decremental ganglion cell. The rod signals are thus similar to those of cones in being divided into separate paths that carry information about increments and decrements of light. They would therefore be expected to reinforce cone responses to intensity variations when both rods and cones are active. However, insofar as the rods feed up the Pc pathway, they would be sending the same signal to opposite sides of mirror-image opponent cell types (see discussion of opponent cells below), and would then have the e ect of decreasing information about color variations. In fact, colors become quite desaturated as light levels decrease.

The discussion above refers only to the straight-through connections from receptors to bipolars to ganglion cells. However, critical to the functioning of the whole system are the lateral interactions made at each synaptic level, through the action of horizontal cells and amacrine cells. In the absence of such interactions, the retinal processing would simply consist of directly relaying the receptor outputs to the brain. This would be pointless because the output of a receptor contains no useful information by itself. It does not identify the color or the brightness in that region; it does not distinguish between a white and a black object or anything about shape

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or motion. Everything of interest to the visual system is contained in the relative activity of di erent receptors, and this is what the neural processing detects and encodes at all visual levels, starting with the receptor-bipolar-horizontal cell synapse.

Horizontal cells interconnect groups of nearby cones, picking up from a group of cones and feeding back into the same group. The horizontal cell processes within the pouches are stimulated by the receptors and also release synaptic transmitters back into the pouches. Each horizontal cell process that connects two or more receptors conducts graded potentials in both directions along its extent, allowing each of the receptors to influence and be influenced by each of the other receptors. The horizontal cell, by that mechanism, responds to the average light level in its local region. Horizontal cells, like receptors, depolarize to decrements and release synaptic transmitters in proportion to their level of depolarization. However, the transmitter released has the e ect of hyperpolarizing the contacted membrane.With this feedback from the horizontal cells, then, the output of a given receptor is not just related to how many photons it is receiving, but rather is proportional to how many photons it is receiving relative to the number being absorbed by the other cones in the near neighborhood. Horizontal cells clearly feed back onto receptors. To what extent they also feed forward onto bipolar cells is not clear. If they do, it poses something of a problem to understand, since the invaginating bipolars, closely juxtaposed to the horizontal cell endings, would presumably be much more a ected than the basal bipolars.

There are two main types of horizontal cells connected with cones in the primate retina. One type interconnects all the L and M cones within a region, but may largely bypass S cones (Anhelt & Kolb, 1994;Wässle, Boycott & Röhrenbeck, 1989). The other type contacts mainly S cones, but some L and M cones, as well. Thus there is no evidence for any specificity in the L/M connectivity (e.g., the feedback to an L cone appears to come from both L and M cones in the region).There appears to be little specificity in the S cone connectivity, as well. A rather similar type of connectivity is present in the inner plexiform layer, where amacrine cells interconnect groups of nearby bipolar cells and feed back to the bipolars, but also feed forward onto ganglion cells.

The receptive field (RF) of a cell is defined as all those receptors which, when stimulated, will activate the cell, or, alternatively, as that region in visual space within which stimuli will activate the cell (see Shapley, chapter 2, this volume). Typically, some stimuli depolarize a cell and lead to an increase in firing; other stimuli hyperpolarize a cell and produce a decrement in firing. The RF organization of a cell, then, is the arrangement of these opposing inputs within the RF extent. The RFs of ganglion cells consist of two opposing inputs: a “center” mechanism and an antagonistic “surround” mechanism. Despite the terms, both of these mechanisms are overlapping and centered on the same receptors. The primary di erence between center and surround is the size of the two regions, the center (generally) being smaller in extent than the surround. The center mechanism in ganglion cells is produced by the direct connections of receptors to bipolars to ganglion cells. The