Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA
Address correspondence to Bevil R. Conway, Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA. Email: bconway{at}hms.harvard.edu.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The issue of which cells in V1 encode color has been obfuscated by the larger debate concerning specialization in the primate visual system. Early studies argued that cells in V1 were specialized to represent only a portion of the visual world (Hubel and Wiesel, 1968). For example, some cells were shown to be strongly selective for the orientation of a stimulus and were thus interpreted to contribute to form perception; other cells were strongly selective for the direction of motion of a stimulus and were therefore thought to contribute to motion perception; and though which cells are responsible for color was not clear, a good candidate was thought to be the dual-opponent cells (Hubel and Wiesel, 1968
; Michael, 1978a
). However, subsequent studies argued that single cells multiplex a representation of multiple aspects of the visual world [e.g. (Leventhal et al., 1995
); for reviews, see works by Gegenfurtner and Lennie (Gegenfurtner and Sharpe 1999
; Lennie, 2000
; Gegenfurtner, 2001
)]. According to this proposal, a single V1 neuron is seen to contribute to our perception of color, form and motion. Despite the obvious limitations of this theory (for example, not all cells in V1 are direction selective, making it difficult to argue that all cells contribute to motion perception), the notion of multi-plexing has been accepted by textbooks (Gegenfurtner and Sharpe 1999
; Lennie, 2000
) and we seem to have lost sight of the obvious specializations (and implications thereof) displayed by cortical neurons.
The idea of multiplexing is especially problematic in the realm of color processing because not all cells show overt cone opponency. And overt cone opponency would seem to be a requirement for a cell to contribute directly to hue discrimination (which we consider a necessary feature of color perception). In fact, only 10% of cells have been shown to respond in an opponent way to opponent colors (e.g. red vs green or blue vs yellow) (Michael, 1978a
,b
; Livingstone and Hubel, 1984
; Tso and Gilbert, 1988
; Conway, 2001
). Moreover, our understanding of the color-coding ability of cortical neurons has been clouded by the use of less-than-optimal stimuli. For example, it is clear that the spatial context of an image shapes color perception (Albers, 1963
) and yet in the pioneering (but only) investigation focusing on the temporal chromatic properties of cortical cells in primate V1, full-field stimuli were used (Cottaris and De Valois, 1998
). Full-field stimuli would have confounded the contribution of spatial context. This confound is made more obviously problematic when one considers the spatial structure of cortical receptive fields. Using quantitative techniques, we recently showed directly that some cortical cell receptive fields are in fact double opponent (Conway, 2001
), confirming earlier, but controversial, claims (Michael, 1978a
). The double opponent name derives from the fact that these cells have both spatially structured and chromatically opponent receptive fields, a feature that makes them extremely likely candidates for the neural basis of spatial color contrast and color constancy (Daw, 1968
; Rubin and Richards, 1982
). Full-field stimuli would have confounded the differing chromatic tuning of receptive-field centers and surrounds of double-opponent cells, making the responses to such stimuli a challenge to interpret.
Color perception shows both spatial (simultaneous) and temporal (sequential) color contrast: red appears redder when surrounded by green or when immediately preceded by green (Hurvich, 1981; Daw, 1987
; Eskew et al., 1994
). Here we re-investigated both spatial and temporal receptive field structure of color cells in V1 of the alert macaque using spatially restricted stimuli (spots). We go further to measure the responses to pairs of colored spots of cone-isolating light, presented both simultaneously and sequentially, to directly address a role for these cells in spatial and temporal color contrast. The results show that only some cells in V1, and not others, could underlie spatial and temporal color contrast. This means that, as far as color is concerned, only a subset of cells in V1 likely contributes to color perception.
![]() |
Materials and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Stimuli were presented (in a dark room) on a computer monitor (Barco Display Systems, Kortrijk, Belgium) 100 cm from the monkeys eyes. Neuron responses were recorded extracellularly using fine electropolished tungsten electrodes coated with vinyl lacquer (Frederick Haer, Bowdoinham, ME) (Hubel, 1957). Action potentials from single neurons were isolated using a dual-window discriminator (BAK Electronics, Germantown, MD) after they were amplified and bandpass filtered (110 kHz). Only well-isolated units were analyzed. All stimuli used to measure the color interactions were cone-isolating and presented on a neutral gray background (see Results). The stimuli that were used to measure the peak L and M response modulation (see Fig. 2
) were generated using high-cone-contrast stimuli, presented on different adapting backgrounds (Conway, 2001
). Methods for generating cone-isolating stimuli, and a discussion of their validity are discussed elsewhere (Estevez and Spekreijse, 1982
; Conway, 2001
).
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Sixty-five cells were classified as color cells: they showed opposite-sign responses (excitation vs suppression) to red (L-isolating) and to green (M-isolating) spots (Fig. 1B, left plot). Because cells were selected for further study based on a screen for L versus M opponency, we were precluded from finding blueyellow cells, which would show the same sign of response to M and L stimuli (assuming blueyellow cells receive inputs from both L and M cones). We did, however, quantify the responses of 12 cells that did not show redgreen opponency (and which we confirmed were not blueyellow cells). We classified these as non-color cells; all of them were orientation-selective complex cells (Hubel and Wiesel, 1968
). Non-color cells gave responses of a similar sign to red and green spots, though the magnitudes of the responses were not always equal so these cells might have been capable of relaying some color information (Fig. 1B
, right plot). But because these cells did not show opponent responses they could not be involved directly in hue discrimination, justifying our designation of them as non-color. It should be emphasized that we only mapped 12 such cells. These were not screened for anything other than lack of cone opponency, yet represent only a small random sample of the non-cone-opponent cells. Regardless, all of the non-color cells responded in a similar way (see Fig. 1C
). For a survey of the chromatic properties of a large sample of cortical cells, the reader is directed to Johnson et al. (Johnson et al., 2001
), Lennie et al. (Lennie et al., 1990
) and Livingstone and Hubel (Livingstone and Hubel, 1984
).
We mapped the spatial and temporal color interactions of 36 color cells and 12 non-color cells. Pairs of cone-isolating stimuli were presented at random locations along a range of locations running through the receptive field center (the stimulus range, Fig. 1A). Color cell receptive fields were sometimes not circularly symmetric, but rather asymmetric or coarsely oriented (Fig. 1C
, left plot) the spatial structure of the receptive fields was determined before mapping the interactions (Conway, 2001
). Thus if a cell had a receptive field that was coarsely oriented, the stimulus range was placed so that the stimuli matched the cells orientation preference and could optimally stimulate the cell. Thousands of frames were used to map a given cell; each frame (e.g. Fig. 1A
) in a given stimulus run was the same duration (between 25 and 100 ms).
Spatial Color Interactions
To determine the simultaneous color interactions, from a continuous history of spike and stimulus timing, we reverse correlated the response to every spatial configuration of the pair of bars along the stimulus range, accounting for the visual latency (Livingstone and Tsao, 1999; Conway, 2001
). The responses are plotted in (xy) coordinates, with zero corresponding to the center of the stimulus range, according to a color scale bar (Fig. 1C
). For example, the maximum firing rate of the color cell shown in Figure 1C
occurred when the L bar was at position 0.75 (x-axis) and the M bar was at 0.5 (y-axis). The arms of the cross in the cone-interaction maps represent the responses of the cell to those occasions when one of the stimuli was in the receptive field and the other was not. For example, the response shown at (0.75, 1.5) was the response of the cell to the L-cone-isolating stimulus in the center of the receptive field and the M-cone-isolating stimulus well outside the receptive field. Note that the cells peak response to the M-cone-isolating stimulus (y = 0.5) was offset to the cells peak response to the L-cone-isolating stimulus (x = 0.75); moreover, there was only one location of peak response to the M-cone-isolating stimulus (shown by the single horizontal band centered on y = 0.5). This is consistent with a single M+/L receptive-field flank, to the left of the L+/M receptive-field center (see the receptive-field schematic for the color cell, Fig. 1C
). Cells that had receptive fields with a single chromatically opponent region [analogous to Type II cells in the lateral geniculate nucleus (Wiesel and Hubel, 1966
)] showed just the horizontal or the vertical arm of the cross.
Twenty out of 36 color cells showed chromatically opponent surround responses, with interaction maps similar to the one in Figure 1C (left plot). In all of these cells, stimulating both center and surround simultaneously, with adjacent red and green spots, elicited stronger activity than stimulating either subregion alone. This was reflected in the cone-interaction maps as increased activity along one or both diagonals parallel to the x = y diagonal, and is shown in the maps as a blob redder than the color in either arm of the cross. In Figure 1C
, left plot, the increase is only below the diagonal, which reflects the presence of only one receptive-field flank. The elevated response to adjacent L and M bars shows directly that these cells are suited to mediate spatial color contrast. All non-color complex cells, on the other hand, showed a completely different response pattern in their interaction maps (Fig. 1C
, right plot): increased activity along the x = y diagonal and decreased activity along flanking diagonals. Thus even though non-color cells can show differently weighted inputs from different cone classes (Fig. 1B
, right plot), they are not suited to color vision: they lack cone opponency (Fig. 1B
, right plot) and they lack the ability to mediate spatial chromatic contrast (Fig. 1C
, right plot). That only 20 of the 36 color cells showed significantly larger responses to adjacent red and green spots reflects the underlying variability in surround strength among color cells (Conway, 2001
).
The simultaneous color interaction maps of all the color cells showed little or no change in activity from baseline along the entire x = y diagonal, indicating that the cells did not respond to overlapping L + M bars (resulting in a yellow stimulus) anywhere in the receptive field. Thus the cells were chromatically opponent throughout the receptive-field center and any surrounding subregions. This cone opponency is clear in Figure 1B, left plot, where the response of the cell to center stimulation with L + M (plotted in yellow) shows little deviation from baseline [unlike the response to center stimulation with L alone (Fig. 1B
, red trace) or M alone (Fig. 1B
, green trace)].
The fact that the response to the yellow stimulus was negligible shows that the responses to L+ and to M+ were not only opponent but also balanced. This is a valid conclusion because the cone contrast of the L and M stimulus were matched (Fig. 1, legend). Thus even though the suppression caused by the M stimulus did not appear as strong as the excitation caused by the L stimulus (possibly because measurement of suppression is limited because the cells firing cannot drop below zero), the suppression by M was strong enough to oppose the strong excitation to L.
Redgreen cells tend to show opponent and balanced responses to L and M, as shown in Figure 2, where higher cone-contrast stimuli, using different colored backgrounds, were used. In Figure 2
, instead of using reduction of firing as a measure of suppression (which can underestimate the extent of suppression because of rectification), we assumed that the suppression was equal in magnitude but opposite in sign to the excitation produced by the opposite-contrast cone-isolating stimulus (Tolhurst and Dean, 1990
; Ferster, 1994
). For example, the suppression by an M+ cone-isolating stimulus (a stimulus that increases the activity of the M cones) would be equal in magnitude, but opposite in sign, to the peak excitation by an M cone-isolating stimulus (a stimulus that decreases the activity of the M cones) (Conway, 2001
). Figure 2
shows the peak center response to the L+ stimulus (x-axis) versus the peak center response to the M stimulus (y-axis) for the L-ON-center cells (squares), and the peak center response to the M+ stimulus (y-axis) versus the peak center response to the L stimulus (x-axis) for the M-ON-center cells (circles). The slope of the relationship between L and M response for the M-ON-center cells is 0.903 (r2 = 0.4); and that for the L-ON-center cells is 1.02 (r2 = 0.3); and that for both populations combined is 0.9 (r2 = 0.9). The slope, which is almost 1, shows that the cells receive almost equal and opposite inputs from L and M cones. The slope may be slightly shallower than 1 because the S-cone contribution, which usually opposes the L-cone contribution in redgreen cells (Conway, 2001
), is not accounted for.
Thus, spatial cone-interaction maps are a useful means of classifying cells in V1. Some cells, which we call color cells, show decreased activity along the x = y diagonal and often show increased activity along flanking diagonals; other cells, which we call non-color cells, show increased activity along the x = y diagonal and decreased activity along the flanking diagonals (Fig. 1C). Color cells show a pattern that suggests they underlie color opponency and spatial color contrast, justifying our designation of these cells as a distinct and specialized class of cell.
Temporal Color Interactions
From the same spike train used to map the simultaneous color interactions, we determined the temporal pattern of response to each color at each location along the stimulus range. This was possible even though two different stimuli were presented in any given frame because the spatial relationship between the stimuli along the stimulus range was random. Thus, by only considering the response to one color stimulus, we averaged out the response to the other color. We confirmed that this was valid by mapping a few cells with just one colored stimulus at a time. Of course it would have been better to map all cells in this way, but it would have taken at least three times as long, and the responses would be from different spike trains. The resulting spacetime maps are analogous to a set of post-stimulus time histograms to stimulation at each point along the stimulus range, where the stimulus range is along the x-axis and the time after stimulation is on the y-axis (Fig. 3AC). Importantly, these maps are distinct from typical reverse-correlation maps because they show the response to every stimulus, regardless of whether or not an action potential occurred. Conventional reverse-correlation maps determine the average stimulus that preceded each action potential. To acknowledge this distinction, these maps are probably better described as forward-correlated, although admittedly that description is cumbersome.
|
Only at the visual latency (50 ms) does the pattern of activity across the stimulus range reflect the cells receptive field. A cell may respond not only to the onset of a stimulus, but also throughout the duration of the stimulus and/or to the cessation of the stimulus. A cells response to the cessation of a stimulus will be represented in the map at a delay corresponding to the sum of the visual latency of the cell (
50 ms) and the duration of the stimulus (25100 ms). Note that we use the term suppression to acknowledge the fact that we do not know the mechanism for the decrease in firing rate: we do not know if it is inhibition or withdrawal of excitation.
All the cells in Figure 3 were color cells; for example, at a short delay, the cell shown in Figure 3A
rarely fired in response to a red spot (asterisk, L map) but often did in response to a green spot (asterisk, M map). Some cells (20/36) showed clear spatial color opponency: in the receptive field region surrounding the center, the pattern of probability was reversed (e.g. Fig. 3B
, arrowhead). The combination of chromatic and spatial opponency earns these cells the designation double opponent; these were the cells that showed increased responses to adjacent red and green spots (Fig. 1C
, left plot). The remaining cells (16/36) showed little sign of spatial opponency: the region surrounding the center was not modulated by >1 SD from the background. These cells may be best described as cortical Type II cells (Wiesel and Hubel, 1966
), though the distinction between Type II and double opponent is somewhat arbitrary because the cells show a range of surround strengths (Conway, 2001
), which may be influenced by the cone contrast of the stimuli.
Color cells often showed not only spatial color opponency but also temporal opponency: most color cells (32/36) that were suppressed by the onset of a stimulus were excited by the cessation of it, while cells that were excited by the onset of a stimulus were usually suppressed by the cessation of it (Motokawa, 1962; Poggio et al., 1975; Livingstone and Hubel, 1984
; Conway, 2001
). For example, the cell shown in Figure 3A
gave an ON response to green spots (asterisk, M map), which was followed by suppression at stimulus cessation (arrow, M map). In contrast, red spots caused suppression, which was followed by a rebound OFF discharge upon stimulus cessation.
The temporal pattern of the responses suggests that these cells might give optimum responses to sequences of appropriately chosen, differently colored spots: the OFF discharge (e.g. center response to red spots, Fig. 3A) might add to or facilitate the ON response to a subsequent stimulus (e.g. the center response to green spots, Fig. 3A
). This modulation could be a mechanism for temporal color contrast: in the same way a briefly flashed red spot appears redder when preceded by a briefly flashed green spot (Eskew et al., 1994
), a red-ON-center cell may be expected to fire more strongly to red when red is preceded by green. In the next set of experiments, we tested for temporal color interactions directly. For the quantitative studies, all stimuli were restricted to the center. For each cell, the stimulus that produced excitation with the shortest latency (in the center of the receptive field) was designated the reference stimulus. Thus for the cell in Figure 3A
the green (i.e. M+-cone-isolating) spot was the reference stimulus. Most color cells (32/36) showed an increase in response to the reference stimulus if the stimulus was immediately preceded by a stimulus of opposite color, red (L+) versus green (M+) (Fig. 3D
). In fact, the response to sequences was predicted by the linear sum of the peak ON response to the reference stimulus plus the peak OFF response to the opposite color (Fig. 3E
; slope = 0.95, r2 = 0.8). This is interesting because modeling efforts of color vision have shown that the machinery responsible for hue discrimination could be linear (Wyszecki and Stiles, 1982
; Hurlbert and Poggio, 1988
). As Figure 3E
shows, color cells, like simple cells in the cat (Ferster, 1994
), blueyellow retinal ganglion cells (Chichilnisky and Baylor, 1999
) and most cells in monkey V1 [(Lennie et al., 1990
); but see De Valois et al. (De Valois et al., 2000
)] do in fact sum their inputs linearly. But, as Wielaard et al. (Wielaard et al., 2001
) have pointed out, the fact that any cortical cell can respond in a linear way is somewhat remarkable given the non-linear nature of the thalamic input and the cortical network itself.
For all 36 cells for which we measured temporal color interactions, we also quantified the percent change of the response to the reference stimulus produced by different preceding stimuli (Fig. 4). A preceding stimulus of opposite color increased the response to the reference stimulus, while a preceding stimulus of identical color decreased the response, as one would expect if these cells were responsible for temporal chromatic contrast (Eskew et al., 1994
). This was not true for non-color cells. In fact, the response of non-color cells to the second (i.e. reference) stimulus of a sequence, regardless of the color of the first stimulus, was always reduced when compared with the response to the reference stimulus presented alone, reminiscent of forward masking of luminance stimuli (Macknik and Livingstone, 1998
).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Some have asked if oriented double-opponent cells multiplex color and direction. A red stimulus moving from a green-ON subregion to a red-ON subregion will elicit an OFF response (from the green subregion) that will sum with the ON response (from the red subregion). But we do not think this indicates that these cells signal direction: the color cells spacetime maps are not slanted [slanted, or spatio-temporally inseparable, space time maps are thought to be fundamental to motion perception (Adelson and Bergen, 1985)] and the direction selectivity of color cells is quantitatively and qualitatively different from that of direction-selective cells (Livingstone et al., 2000
) (B.R. Conway and M.S. Livingstone, submitted for publication). Furthermore, even if these orientation-selective cone-opponent cells could multiplex color and direction, are there enough of them to represent the entire visual world? Probably not given that the total sum of all cortical color-opponent cells, in all their manifestations, would barely be sufficient to encompass the entire visual world (we estimate that they account for <10% of cortical cells). So, if cortical cells genuinely do not multiplex color, form and direction, then how do we achieve a unified perception of the visual world? Perhaps subsequent visual areas sample from the various specialized populations of cells in V1 [and there is ample evidence that this is true: Van Essen et al. (Van Essen et al., 1992
)]. Thus in the same way trichromacy exists at the earliest stage of visual processing but subsequently gives rise to opponency, so specialization exists in V1 but subsequently gives rise to multiplexing.
In summary, the choices of stimuli that we make will ultimately shape how clearly various physiological specializations can be seen. Thus there is a tradeoff between doing large population studies, where large numbers of cells are mapped with a small battery of stimuli and one risks gaining only a muddy appreciation of the various cortical specializations, and screening for cells using specialized stimuli, where one risks making inaccurate descriptions about the total population of cortical cells. Perhaps it is an appreciation of the benefit of both types of studies that is leading to a convergent understanding of the mechanism of color processing in V1 (Conway, 2001; Engel and Furmanski, 2001
; Johnson et al., 2001
).
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Albers J (1963) Interaction of color. New Haven, CT: Yale University Press.
Baylor DA, Nunn BJ, Schnapf JL (1987) Spectral sensitivity of cones of the monkey Macaca fascicularis. J Physiol 390:145160.[Abstract]
Chichilnisky EJ, Baylor DA (1999) Receptive-field microstructure of blueyellow ganglion cells in primate retina. Nat Neurosci 2:889893.[ISI][Medline]
Conway BR (2001) Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1). J Neurosci 21:27682783.
Cottaris NP, De Valois RL (1998) Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 395:896900.[ISI][Medline]
Dacey DM, Lee BB (1994) The blue-on opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367:731735.[ISI][Medline]
Daw N (1968) Goldfish retina: organization for simultaneous color contrast. Science 158:942944.[ISI]
Daw NW (1987) Color vision. In: Encyclopedia of neuroscience (Adelman G, ed.), pp. 259260.
De Valois RL, Morgan HC, Polson MC, Mead WR, Hull EM (1974) Psychophysical studies of monkey vision. I. Macaque luminosity and color vision tests. Vision Res 14:5367.[ISI][Medline]
De Valois RL, Cottaris NP, Elfar SD, Mahon LE, Wilson JA (2000) Some transformations of color information from lateral geniculate nucleus to striate cortex. Proc Natl Acad Sci USA 97:49975002.
Donner KO, Rushton WAH (1959) Retinal stimulation by light substitution. J Physiol 149:288302.[ISI]
Engel SA, Furmanski CS (2001) Selective adaptation to color contrast in human primary visual cortex. J Neurosci 21:39493954.
Eskew RT, Stromeyer CF, Kronauer RE (1994) Temporal properties of the redgreen chromatic mechanism. Vision Res 34:31273137.[ISI][Medline]
Estevez O, Spekreijse H (1982) The silent substitution method in visual research. Vision Res 22:681691.[ISI][Medline]
Ferster D (1994) Linearity of synaptic interactions in the assembly of receptive fields in cat visual cortex. Curr Opin Neurobiol 4:563568.[Medline]
Gegenfurtner K. (2001) Color in the cortex revisited. Nat Neurosci 4:339340.[ISI][Medline]
Gegenfurtner KR, Sharpe LT (1999) Color vision: from genes to perception. Cambridge: Cambridge University Press.
Gouras P, Kruger J (1979) Responses of cells in foveal visual cortex of the monkey to pure color contrast. J Neurophysiol 42:850860.
Hering E (1964) [translated by Hurvich LM, Jameson D] Outlines of a theory of the light sense. Cambridge, MA: Harvard University Press.
Hubel DH (1957) Tungsten microelectrode for recording from single units. Science 125:549.[ISI]
Hubel DH, Livingstone MS (1990) Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey. J Neurosci 10:22232237.[Abstract]
Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195:215243.[ISI][Medline]
Hurlbert AC, Poggio TA (1988) Synthesizing a color algorithm from examples. Science 239:482485.[ISI][Medline]
Hurvich LM (1981) Color vision. Sunderland, MA: Sinauer Associates.
Johnson EN, Hawken MJ, Shapley RM (2001) The spatial transformation of color in the primary visual cortex of the macaque monkey. Nat Neurosci 4:409416.[ISI][Medline]
Lennie P (2000) Color vision. In: Principles of neural science, 4th edn (Kandel ER, Schwartz JH, Jessel TM, eds), p. 583. New York: McGraw Hill.
Lennie P, Krauskopf J, Sclar G (1990) Chromatic mechanisms in striate cortex of macaque. J Neurosci 10:649669.[Abstract]
Leventhal AG, Thompson KG, Liu D, Zhou Y, Ault SJ (1995) Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex. J Neurosci 15:18081818.[Abstract]
Livingstone ML, Conway BR, Tsao DY (2000) What happens when it changes contrast when it moves? Soc Neurosci Abstr 26:162.6.
Livingstone MS (1998) Mechanisms of direction selectivity in macaque V1. Neuron 20:509526.[ISI][Medline]
Livingstone MS, Hubel DH (1984) Anatomy and physiology of a color system in the primate visual cortex. J Neurosci 4:309356.[Abstract]
Livingstone MS, Hubel DH (1987) Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J Neurosci 7:34163468.[Abstract]
Livingstone MS, Tsao DY (1999) Receptive fields of disparity-selective neurons in macaque striate cortex. Nat Neurosci 2:825832.[ISI][Medline]
Livingstone MS, Freeman DC, Hubel DH (1996) Visual responses in V1 of freely viewing monkeys. Cold Spring Harb Symp Quant Biol 61:2737.[ISI][Medline]
Macknik SL, Livingstone MS (1998) Neuronal correlates of visibility and invisibility in the primate visual system. Nat Neurosci 1:144149.[ISI][Medline]
Michael, CR (1978a) Color vision mechanisms in monkey striate cortex: dual-opponent cells with concentric receptive fields. J Neurophysiol 41:572588.
Michael, CR (1978b) Color vision mechanisms in monkey striate cortex: simple cells with dual opponent color receptive fields. J Neurophysiol 41:12331249.
Motokawa K, Taira N, Okuda J (1962) Spectral responses of single units in the primate visual cortex. Tohoku J Exp Med 78:320337.[ISI]
Mullen KT (1985) The contrast sensitivity of human colour vision to redgreen and blueyellow chromatic gratings. J Physiol 359: 381400.[Abstract]
Poggio GF, Baker FH, Mansfield RJ, Sillito A, Grigg P (1975) Spatial and chromatic properties of neurons subserving foveal and parafoveal vision in rhesus monkey. Brain Res 100:2559.[ISI][Medline]
Reid RC, Shapley RM (1992) Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature 356:716718.[ISI][Medline]
Roorda A, Williams DR (1999) The arrangement of the three cone classes in the living human eye. Nature 397:520522.[ISI][Medline]
Rubin JM, Richards WA (1982) Color vision and image intensities: when are changes material? Biol Cybern 45:215226.[ISI][Medline]
Sandell JH, Gross CG, Bornstein MH (1979) Color categories in macaques. J Comp Physiol Psychol 93:626635.[ISI][Medline]
Smith VC, Pokorny J (1975) Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Res 15:161171.[ISI][Medline]
Stockman A, Sharpe LT (2000) Tritanopic color matches and the middle- and long-wavelength-sensitive cone spectral sensitivities. Vision Res 40:17391750.[ISI][Medline]
Tailor DR, Finkel LH, Buchsbaum G (2000) Color-opponent receptive fields derived from independent component analysis of natural images. Vision Res 40:26712676.[ISI][Medline]
Thorell LG, De Valois RL, Albrecht DG (1984) Spatial mapping of monkey V1 cells with pure color and luminance stimuli. Vision Res 24:751769.[ISI][Medline]
Tolhurst DJ, Dean AF (1990) The effects of contrast on the linearity of spatial summation of simple cells in the cats striate cortex. Exp Brain Res 79:582588.[ISI][Medline]
Tso DY, Gilbert CD (1988) The organization of chromatic and spatial interactions in the primate striate cortex. J Neurosci 8:17121727.[Abstract]
Van Essen DC, Anderson CH, Fellemen DJ (1992) Information processing in the primate visual system: an integrated systems perspective. Science: 419423.
Wachtler T, Lee TW, Sejnowski TJ (2001) Chromatic structure of natural scenes. J Opt Soc Am A 18:6577.[ISI]
Wandell BA (1995) Foundations of vision. Sunderland, Massachusetts: Sinauer Associates.
Wielaard DJ, Shelley M, McLaughlin D, Shapley RM (2001) How simple cells are made in a nonlinear network model of the visual cortex. J Neurosci 21:52035211.
Wiesel TN, Hubel DH (1966) Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J Neurophysiol 29:1115156.
Wyszecki G, Stiles WS (1982) Color science: concepts and methods, quantitative data and formulae. New York: John Wiley.
Zeki S, Aglioti S, McKeefry D, Berlucchi G (1999) The neurological basis of conscious color perception in a blind patient. Proc Natl Acad Sci USA 96:1412414139.