Standard definitions of chromatic induction fail to describe induction with S-cone patterned backgrounds

Inducing patterns that selectively stimulate the S cones can induce large shifts in color appearance. For example, a “peach” test-ring presented within contiguous purple and non-contiguous lime inducing rings appears pink while the physically identical peach test-ring appears orange when presented within contiguous lime and non-contiguous purple inducing rings (Fig. 1c). These shifts have been accounted for by a neural substrate which predicts that chromatic assimilation and simultaneous contrast can operate synergistically to produce large shifts with these patterns [Monnier, P., & Shevell, S. K. (2004). Chromatic induction from S-cone patterns. Vision Research, 44, 849-856].Here, induction was measured for test-rings that stimulated the S cones either more or less than did the inducing rings. According to standard definitions of induction, color shifts for test s-chromaticities either lower or higher than both inducing chromaticities should be attenuated compared to test-rings of intermediate S-cone stimulation. On the other hand, a previously proposed model of induction predicted independence of the color shifts with test-ring s-chromaticity. Consistent with standard definitions of induction, a reduction in the magnitude of the color shifts for test-ring chromaticities either lower or higher in S-cone excitation than the inducing chromaticities was observed. Additional measurements with patterns that have been shown to isolate assimilation and simultaneous contrast were conducted. For these patterns, expectations based on standard definitions of induction suggested that the magnitude of the color shifts should be monotonic with the S-cone stimulation of the test-ring, and the direction of the color shift should reverse for test-ring chromaticities either lower or higher than both inducing chromaticities compared to test-rings of intermediate chromaticity. In contrast, the previously proposed model of induction based on a receptive-field with S-cone spatial antagonism predicted the color shifts should be independent of the test-ring chromaticity (Monnier & Shevell, 2004). Color shifts were generally independent of the level of the test-ring chromaticity, supporting the S-cone antagonistic model of induction.     

Chromatic induction from S-cone patterns

Chromatic induction from patterned backgrounds depends on the spatial as well as the chromatic aspects of the background light. Color appearance with patterned and uniform backgrounds was compared using chromaticities distinguished by only the S cones; all backgrounds were equivalent to equal-energy white in terms of L-cone and M-cone stimulation. The measurements showed larger shifts in color appearance with a patterned chromatic background than with a uniform background at any chromaticity within the pattern. The measurements also showed that inducing light within different spatial regions could cause opposite shifts in color appearance: inducing light near a test field shifted appearance toward the inducing chromaticity (assimilation), while the same light some distance from the test shifted appearance away from the inducing chromaticity (simultaneous contrast). The shifts in color appearance were accounted for by a neural receptive field with S-cone spatial antagonism.     

Temporal nulling of induction from spatial patterns modulated in time

Temporally varying chromatic-inducing light was used to infer receptive-field organization. Time-varying shifts in color appearance within a test field were induced by a surrounding chromatic pattern; the shifts were then nulled by adding a time-varying stimulus to the test area so the observer perceived a steady test. This method measured chromatic induction without requiring an observer to judge the color appearance of the test. The induced color shifts were consistent with a +s/-s spatially antagonistic neural receptive field, which also accounts for color shifts induced by static chromatic patterns (Monnier & Shevell, 2003, Monnier & Shevell, 2004). The response of this type of receptive-field, which is found only in the visual cortex, increases with S-cone stimulation at its center and decreases with S-cone stimulation within its surround. The measurements also showed a negligible influence of temporal inducing frequency in the range 0.5-4 Hz.     

Color shifts from S-cone patterned backgrounds: contrast sensitivity and spatial frequency selectivity

Patterned backgrounds that selectively stimulate the S-cones cause conspicuous color shifts. These shifts are accounted for by an S-cone antagonistic (+S/-S) center-surround receptive field [Monnier, P., & Shevell, S. K. (2004). Chromatic induction from S-cone patterns. Vision Research, 44, 849-856]. The present study tested two additional implications of the S-cone receptive field for color shifts: (1) proportionality of the shifts with respect to S-cone contrast within the inducing pattern and (2) bandpass selectivity of the shifts with respect to the spatial frequency of the inducing pattern. Measurements showed that the magnitude of the color shift was linear with S-cone contrast and that the largest color shift was observed with inducing patterns at an intermediate spatial frequency. These results further support an S-cone spatially antagonistic receptive field as the neural substrate mediating the large color shifts from S-cone patterns.     

Cone weights for the two cone-opponent systems in peripheral vision and asymmetries of cone contrast sensitivity

In understanding the basis of the changes in human color vision across eccentricity, one key piece of information remains unknown, whether the relative cone weights of the two cone opponent mechanisms vary. Here we measure detection threshold contours within three planes in a 3-dimensional cone contrast space to reveal the L, M and S-cone weights to the two cone opponent mechanisms, L/M and S/(L+M). We find these remain constant across eccentricity suggesting the underlying structures of the cone opponent mechanisms are invariant. The contrast sensitivities of two poles of the S-cone opponent mechanism also remain symmetrical, whereas small asymmetries develop in L/M opponency from about 15 degrees.     

Simultaneous S-cone contrast.

Chromatic induction is the change in appearance of one light caused by a second, nearby light. We measured chromatic induction in a central test viewed within an inducing field that was varied in only short-wavelength-sensitive (S) cone stimulation. The observer matched the appearance of the central test by adjusting the chromaticity of a haploscopically presented comparison field, seen by the other eye on a dark background. When the central test weakly stimulated S cones, the S-cone level in the surround caused little change in the color appearance of the test. When the central test substantially stimulated S cones, on the other hand, the appearance of the center showed S-cone contrast: raising the level of S in the surround reduced the level of S set to match the central test. Further, a surround that weakly stimulated S cones raised the matching S-cone level above that required without a surround (dark-adapted condition). These results cannot be explained by S-cone sensitivity loss or by a two-process model of adaptation. A cortical mechanism is proposed to mediate S-cone antagonism.     

The pupil's response to short wavelength cone stimulation

Using i.r. pupillometry, we measured the response of the pupil to tritanopic metamers alternating at 0.94 Hz. These are lights that differentially stimulate only the short wavelength (S) sensitive cones. We find a response at the alternation frequency for 5 of 7 observers. This shows, for the 5 observers, that S cone signals can influence pupil size, probably via the traditional retinotectal light reflex pathway. Changing the radiance of just one of the alternating pair of lights causes the two lights to differ in their total M + L cone stimulation. The pupil's response to this imbalance can antagonize its response to S cone stimulation. By this procedure we find that imbalances in M + L cone stimulation of less than 0.3 log10 unit offset the pupil's response to S cone stimulation of more than 0.8 log10 unit. This suggests that afferent pupillary signals from S cones are weak relative to those from M + L cones.     

Induction from a below-threshold chromatic pattern

Patterned backgrounds can induce large shifts in color appearance, even with patterns of only 10% S-cone contrast (S. K. Shevell & P. Monnier, 2005). The present study tested whether a background pattern could induce color shifts even at a below-threshold contrast. In the first experiment, S-cone contrast threshold for discriminating a pattern from a homogenous background was measured by a 2AFC procedure. Next, a test ring was inserted within the patterned background. With the test ring present, six of eight observers reliably distinguished trials with a patterned background from trials with a homogeneous field, even though the S-cone contrast in the pattern was too low to be discriminated from a homogeneous background. This suggested that a below-threshold S-cone pattern shifted the color appearance of the test ring; that is, the appearance of the test was used to discriminate whether the background was patterned or homogeneous. This was corroborated by asymmetric color matches, which revealed a color shift caused by subthreshold S-cone contrast within the patterned background.     

Dark-adapted rod suppression of cone flicker detection: Evaluation of receptoral and postreceptoral interactions

Dark-adapted rods in the area surrounding a luminance-modulated field can suppress flicker detection. However, the characteristics of the interaction between rods and each of the cone types are unclear. To address this issue, the effect that dark-adapted rods have on specific classes of receptoral and postreceptoral signals was determined by measuring the critical fusion frequencies (CFF) for receptoral L-, M-, and S-cone and postreceptoral luminance ([L+M+S] and [L+M+S+Rod]) and chromatic ([L/(L+M)]) signals in the presence of different levels of surrounding rod activity. Stimuli were generated with a two-channel photostimulator that has four primaries for a central field and four primaries for the surround, allowing independent control of rod and cone excitation. Measurements were made either with adaptation to the stimulus field after dark adaptation or during a brief period following light adaptation. The results show that dark-adapted rods maximally suppressed the CFF by approximately 6 Hz for L-cone, M-cone, and luminance modulation. Dark-adapted rods, however, did not significantly alter the S-cone CFF. The [L/(L+M)] postreceptoral CFF was slightly suppressed at higher surround illuminances, that is, higher than surround luminances resulting in suppression for L-cone, M-cone, or luminance modulation. We conclude that rod-cone interactions in flicker detection occurred strongly in the magnocellular pathway.     

Chromatic discrimination in the presence of incremental and decremental rod pedestals

Signals from rods can alter chromatic discrimination. Here, chromatic discrimination ellipses were determined in the presence of rod incremental and decremental pedestals at mesopic light levels. The data were represented in a relative cone Troland space, normalized by discrimination thresholds measured along the cardinal axes without a rod pedestal. In the quadrant of cone space where L-cone relative to M-cone excitation increased, and S-cone excitation decreased, rod incremental pedestals degraded chromatic discrimination, and rod decremental pedestals improved chromatic discrimination. Discrimination in the other three quadrants of cone space was unaffected by the incremental or decremental rod pedestals. A second experiment measured chromatic discrimination under conditions where cone pedestals were matched to the appearances of the incremental and decremental rod pedestals. Based on the matching pedestal data, discrimination then could be measured independently along the cardinal axes using either chromatic [L/(L + M); S/(L + M)] or luminance (L + M) pedestal components. The discrimination data altered by the rod pedestals were similar to chromatic cone pedestals for L/M increment discrimination, but similar to luminance cone pedestals for S decrement discrimination. The results indicated that the rod and cone signals combined differently in determining chromatic discrimination for different post-receptoral pathways.     

Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina

The topography of medium (M)- and short (S)-wavelength sensitive cone photoreceptors was studied in the domestic pig retina. Antisera specific for M or S opsin as well as cone photoreceptor proteins arrestin and alpha-transducin were used to label cone types. Retinal wholemounts and their blood vessel patterns were drawn and specific regions removed. The wholemounts were immunocytochemically labelled to detect both M and S cones, and the specific regions labelled to detect S cones. Cones were counted in a 1 mm grid pattern, using the drawings as a guide. Pig retina has a high cone density retinal streak extending across the retina covering the optic disc (OD) and horizontal meridian. Densities in the streak are 20,000-35,000 mm(-2). Two higher peaks occur in the streak, one in temporal retina near the OD (39,000 mm(-2)) and the other in nasal retina 5-7 mm from the OD (40,500 mm(-2)). The lowest cone density is in far peripheral inferior retina (7000 mm(-2)). The total number of cones in pig retina is 17-20 million. Both types of cones are found throughout the retina, with S cone percentages ranging from 7.4 to 17.5% in no consistent topographical pattern. S cones have an irregular local distribution which can vary from a regular hexagonal pattern to small clusters of adjacent S cones to small areas lacking S cones. Double-label immunocytochemistry found that virtually all S cone outer segments (OS) contain some M opsin. M cone OS do not label at detectible levels for S opsin. Domestic pig retina is widely available, large, has a high cone density and has two types of cones. This tissue should be an excellent source for biochemical analysis of cone proteins, and for in vitro approaches to understanding cone survival factors.     

Trichromatic reconstruction from the interleaved cone mosaic: Bayesian model and the color appearance of small spots

Observers use a wide range of color names, including white, to describe monochromatic flashes with a retinal size comparable to that of a single cone. We model such data as a consequence of information loss arising from trichromatic sampling. The model starts with the simulated responses of the individual L, M, and S cones actually present in the cone mosaic and uses these to reconstruct the L-, M-, and S-cone signals that were present at every image location. We incorporate the optics and the mosaic topography of individual observers, as well as the spatio-chromatic statistics of natural images. We simulated the experiment of H. Hofer, B. Singer, & D. R. Williams (2005) and predicted the color name on each simulated trial from the average chromaticity of the spot reconstructed by our model. Broad features of the data across observers emerged naturally as a consequence of the measured individual variation in the relative numbers of L, M, and S cones. The model's output is also consistent with the appearance of larger spots and of sinusoidal contrast modulations. Finally, the model makes testable predictions for future experiments that study how color naming varies with the fine structure of the retinal mosaic.     

The spectral sensitivity of the human short-wavelength sensitive cones derived from thresholds and color matches.

We used two methods to estimate short-wave (S) cone spectral sensitivity. Firstly, we measured S-cone thresholds centrally and peripherally in five trichromats, and in three blue-cone monochromats, who lack functioning middle-wave (M) and long-wave (L) cones. Secondly, we analyzed standard color-matching data. Both methods yielded equivalent results, on the basis of which we propose new S-cone spectral sensitivity functions. At short and middle-wavelengths, our measurements are consistent with the color matching data of Stiles and Burch (1955, Optica Acta, 2, 168-181; 1959, Optica Acta, 6, 1-26), and other psychophysically measured functions, such as pi 3 (Stiles, 1953, Coloquio sobre problemas opticos de la vision, 1, 65-103). At longer wavelengths, S-cone sensitivity has previously been over-estimated.     

The influence of color on the perception of luminance motion

We examined the role of color in the processing of motion of a luminance-varying pattern by alternating the color of a moving pattern and measuring the luminance contrast required for accurate discrimination of the motion direction. We report that the contrast threshold for perceiving the direction of motion of luminance-varying patterns is greatly elevated when the mean chromaticity of the moving luminance pattern alternates between two hues. Thus, color plays a critical role in the discrimination of luminance motion direction. The magnitude of the threshold elevation is directly related to the magnitude of the LM opponent color contrast produced by the color alternation. S-cone contrast produces little or no effect. The interference produced by color alternation was greatly reduced in the retinal periphery. Our results indicate that first-order luminance motion mechanisms are sensitive to the color of moving objects as coded by a differencing of the outputs of L and M cones. Contrary to the widely accepted notion that luminance-defined motion is processed primarily in the spectrally broadband magnocellular (M) pathway, our results suggest that the hue-selective parvocellular (P) mechanisms provide input to first-order motion detectors.     

Cone-specific mediation of rod sensitivity in trichromatic observers

PURPOSE: The slope of the rod threshold versus the illuminance (TVI) function changes with the wavelength of the background light. This study was conducted to determine whether the changes in slope are due to the stimulation of specific cone classes. METHODS: An eight-channel optical system was used to generate lights that differed in cone and rod photoreceptor illuminance. Rod flicker TVI functions were measured in normal trichromatic observers at mesopic light levels. The independent variables were (1) the relative contribution of the short (S)- and long (L)- wavelength cones to the background light (i.e., the background lights varied along S-only and L-only lines), and (2) the temporal frequency of the flickering lights (4, 7.5, and 15 Hz). RESULTS: The 4-Hz rod flicker TVI function had a slope of 0.87 when measured near W (MacLeod-Boynton chromaticity of 0.66, 1.0). At 4 and 7.5 Hz, an increase in the relative L-cone illuminance steepened the slope of the rod-only TVI curve, but an increase in the relative S-cone illuminance had no effect. The slope of the 7.5-Hz TVI function decreased at higher illuminance levels. At 15 Hz, the thresholds could be measured over only a limited range. CONCLUSIONS: The L-cone system contributes to the desensitization of the rod system at mesopic light levels, whereas, in the range of lights used in these experiments, the S-cone system apparently does not. The possibility that S-cone stimulation desensitizes the response to rod signals at higher levels of S-cone illumination cannot be eliminated.     

Differential attentional modulation of cortical responses to S-cone and luminance stimuli

Neural signals driven by short-wave-sensitive (S) cones are, to a large degree, anatomically and functionally separate from the achromatic luminance pathway until at least one synapse into V1. Attentional mechanisms that act at an anatomically early stage in V1 may, therefore, affect S-cone and luminance signals differently. Here, we used a steady-state visually evoked potential (SSVEP) paradigm combined with electrical source imaging to study the effects of contrast and attention on neural responses to both chromatic S-cone isolating and achromatic stimuli in five human visual areas including V1. The responses to these gratings were affected very differently by changes in contrast and attention. Increasing cone contrast increased the response amplitude for both types of stimulus. For the S-cone-defined stimuli, we also observed a systematic decrease in the response phase of the first harmonic with increasing stimulus contrast, but there was no corresponding change in phase for the first harmonic of the luminance probes. Attending to the contrast of the grating increased the amplitude and phase of luminance-driven responses but had no effect on S-cone-driven responses. We conclude that while attentional modulation can be observed in achromatic pathways as early as V1, attention may not affect SSVEP signals generated by S-cone stimuli.     

Rods induce transient tritanopia in blue cone monochromats.

Transient tritanopia is a cone-cone post-receptoral interaction between short-wavelength (S) cones and medium (M) and long (L) wavelength cones. Blue cone monochromats have rods and S cones of normal sensitivity but lack functional M/L cones. All blue cone monochromats tested (n = 8) show significant amounts of transient tritanopia mediated by rods. Attempts to find a similar rod-S cone interaction while silencing the L/M cones in normals yielded only a small amount of S cone sensitivity loss. The results suggest an exaggerated influence of rods on the S cone pathway in the retina of blue cone monochromats.     

The role of opsin expression and apoptosis in determination of cone types in human retina

In primates, short wavelength sensitive cones (S cones) and medium- or long-wavelength-sensitive cones (L/M cones) are two separate populations. Each cone type has a different developmental timecourse, contributes to different intra-retinal circuits, and transmits different types of information to the brain. However, in fetal human retina a significant population of cones express both S and L/M opsin (S+L/M cones), raising questions about whether S+L/M cones die or change opsin expression during development. We have utilized fetal, postnatal and adult human retinae to study the immunohistochemical distribution and morphology of S+L/M cones during development. Because S cones appear to be at higher density in fetal compared to adult retinae, we used antibodies to S opsin and alpha-transducin to estimate the proportion of S-cones, and TUNEL labelling to detect apoptotic death in the L/M, S or S+L/M population during development. S cones were present in central retina from fetal week (Fwk)11 and covered the retina by Fwk20. L/M cones appeared in the foveal cone mosaic 3-4 weeks after S-opsin was first detected, and covered the retina by birth. S+L/M cones were detected in all retinae older than Fwk14. They were most numerous at the retinal eccentricity where L/M opsin was just appearing; i.e. at the 'front' of L/M opsin expression. In this region, five morphological types of cones were present. (1) Heavily labelled S cones had thick cell bodies, a thick basal axon and pedicle, and a nucleus at any level of the outer nuclear layer (ONL). (2) Heavily labelled L/M cones were wine goblet shaped with a small round cell body, a large nucleus at the outer ONL edge, and a thin axon with a prominent synaptic pedicle. (3) Goblet-shaped S+L/M cones. (4) Goblet-shaped cones lightly labelled for S-opsin. (5) Cones that were not immunoreactive to either opsin. Only type 1 S cones were present peripheral to the L/M expression front, and their labelling intensity, morphology and distribution indicates that these are the 'true blue' cones of the adult mosaic. Only type 2 L/M cones were present in the foveal cone mosaic. Types 3 and 4 were most numerous within 500-750 microm of the L/M expression front, but type 3 S+L/M cones were also scattered throughout more central regions in fetal, infant and adult retinae. S+L/M cones comprised 5-10% of opsin immunoreactive cones at the L/M front in fetal and early postnatal retinas but 0.01-0.03% throughout P8mo and adult retinae. We found no evidence of significant levels of apoptosis in L/M cones at the expression front, suggesting that this decrease was not due to cell death. The findings suggest that goblet-shaped cones destined to express L or M opsin may initially and transiently express S opsin. Near the optic disc, at Fwk17 S cone density was around 2000 cells mm(-2), which dropped 50% by Fwk20 and stabilized at around 500 cells mm(-2) by birth. Double labelling with alpha-transducin showed that throughout this period 8-10% of all cones expressed S opsin. TUNEL labelling found no significant apoptosis in the S cone population. The decrease in S cone density near the optic disc occurs in the absence of apoptosis, and is likely due to other developmental events acting on the photoreceptor layer, including displacement of cones towards the fovea.     

Seeing with S cones

The S cone is highly conserved across mammalian species, sampling the retinal image with less spatial frequency than other cone photoreceptors. In human and monkey retina, the S cone represents typically 5-10% of the cone mosaic and distributes in a quasi-regular fashion over most of the retina. In the fovea, the S cone mosaic recedes from a central "S-free" zone whose size depends on the optics of the eye for a particular primate species: the smaller the eye, the less extreme the blurring of short wavelengths, and the smaller the zone. In the human retina, the density of the S mosaic predicts well the spatial acuity for S-isolating targets across the retina. This acuity is likely supported by a bistratified retinal ganglion cell whose spatial density is about that of the S cone. The dendrites of this cell collect a depolarizing signal from S cones that opposes a summed signal from M and L cones. The source of this depolarizing signal is a specialized circuit that begins with expression of the L-AP4 or mGluR6 glutamate receptor at the S cone-->bipolar cell synapse. The pre-synaptic circuitry of this bistratified ganglion cell is consistent with its S-ON/(M+L)-OFF physiological receptive field and with a role for the ganglion cell in blue/yellow color discrimination. The S cone also provides synapses to other types of retinal circuit that may underlie a contribution to the cortical areas involved with motion discrimination.     

Tetrachromatic input to turtle horizontal cells

Recent physiological experiments support behavioral and morphological evidence for a fourth type of cone in the turtle retina, maximally sensitive in the ultraviolet (UV). This cone type has not yet been included in the models proposed for connectivity between cones and horizontal cells. In this study, we examined the inputs of UV, S, M, and L cones to horizontal cells. We used the high-resolution Dynamic Constant Response Method to measure the spectral sensitivity of horizontal cells without background light and after adaptation to UV, blue (B), green (G), and red (R) light. We concluded the following: (1) Tetrachromatic input to a Y/B horizontal cell was identified. The spectral-sensitivity curves of the cell in three of the adaptation conditions were well represented by L-, M-, and S-cone functions. Adaptation to blue light revealed a peak at 372 nm, the same wavelength location as that determined behaviorally in the turtle. A porphyropsin template could be closely fitted to the sensitivity band in that region, strong evidence for input from a UV cone. (2) The spectral-sensitivity functions of R/G horizontal cells were well represented by the L- and M-cone functions. There was no indication of UV- or S-cone inputs into these cells. (3) The spectral sensitivities of the monophasic horizontal cells were dominated by the L cone. However, the shape of the spectral-sensitivity function depended on the background wavelength, indicating secondary M-cone input. Connectivity models of the outer retina that predict input from all cone types are supported by the finding of tetrachromatic input into Y/B horizontal cells. In contrast, we did not find tetrachromatic input to R/G and monophasic horizontal cells. Chromatic adaptation revealed the spectral-sensitivity function of the turtle UV cone peaking at 372 nm.