Biomedical subjects
Publications and source records attributed to D I MacLeod.
Through unique observations of an adult case of bilateral congenital cataract removal, we have found evidence that retinal photoreceptors will swiftly realign towards the brightest regions in the pupils of the eye. Cones may be phototropic, actively orientating themselves towards light like sunflowers in a field.
Exposure to visual patterns of high contrast (for example, gratings formed by alternating white and black bars) creates after-effects in perception. We become temporarily insensitive to faint test patterns that resemble the pre-exposed pattern (such as gratings of the same orientation), and we require more contrast to detect them. Moreover, if the test pattern is slightly tilted relative to the pre-exposed one, this tilt may be perceptually exaggerated: we experience a tilt after-effect. Here we show that these visual after-effects occur even if the pre-exposed grating is too fine to be perceptually resolved. After looking at a very fine grating, so high in spatial frequency that it was perceptually indistinguishable from a uniform field, observers required more contrast to detect a test grating presented at the same orientation than one presented at the orthogonal orientation. They also experienced a tilt after-effect that depended on the relation of the test pattern's tilt to the unseen orientation of the pre-exposed pattern. Because these after-effects are due to changes in orientation-sensitive mechanisms in visual cortex, our observations imply that extremely fine details, even those too fine to be seen, can penetrate the visual system as far as the cortex, where they are represented neurally without conscious awareness.
To determine whether vision with obliquely incident light is degraded by contrast losses originating in the retina, laser interference fringe patterns were produced on the retina for various directions of incidence of the two interfering beams. Contrast-modulation flicker [Vision Res. 38, 985 (1998)] was used as a psychophysical measure of contrast at the level of the photoreceptors. Fringe contrast was shown to be maximal when the interfering beams were equal in perceived brightness, not in physical intensity. The effective fringe contrast was slightly reduced with oblique incidence for high spatial frequencies, but the reduction was too slight to be an important factor in visual resolution. The loss was similar whether the incident beams were displaced from the pupil center in a direction parallel or perpendicular to the grating bars.
We discuss how visual nonlinearity can be optimized for the precise representation of environmental inputs. Such optimization leads to neural signals with a compressively nonlinear input-output function the gradient of which is matched to the cube root of the probability density function (PDF) of the environmental input values (and not to the PDF directly as in histogram equalization). Comparisons between theory and psychophysical and electrophysiological data are roughly consistent with the idea that parvocellular (P) cells are optimized for precision representation of colour: their contrast-response functions span a range appropriately matched to the environmental distribution of natural colours along each dimension of colour space. Thus P cell codes for colour may have been selected to minimize error in the perceptual estimation of stimulus parameters for natural colours. But magnocellular (M) cells have a much stronger than expected saturating nonlinearity; this supports the view that the function of M cells is mainly to detect boundaries rather than to specify contrast or lightness.
Little is known about the mechanism that regulates the sensitivity of rod system at its normal operating light levels. Two experiments are reported in this paper. First, we searched for nonlinear distortion products in rod vision that could be generated from any local adaptation process, using a sensitive experimental procedure that has demonstrated local adaptation in cone vision. No local adaptation was evident in the rod system, even at near saturating light levels. Second, to investigate the dynamics of light adaptation in the rod system we presented a uniform flickering background, sinusoidally modulated in time, and measured increment thresholds for brief test flashes that were superimposed on this background at different times during the sinusoidal flicker cycle. At frequencies less than 5-6 Hz, the rod increment threshold follows the background modulation, with a slight phase advance. When the background is modulated faster than 5-6 Hz, the increment threshold remains the same regardless of when the test flash occurred during the background cycle. Thus the rod system sensitivity, unlike that of the cone system, can only change slowly, and is set by a space-integrated signal rather than independently for different rods.
The gamut of perceived colors can be represented in a space with bright-dark, red-green and blue-yellow axes. Pre-exposure to a field that changes periodically over time in luminance or along one of the color axes reduces vividness of colors along the entire axis [Webster and Mollon (1991) Nature, 349, 235-238]. But is it possible to reduce vividness or perceived contrast selectively for half-axes in color space? We assessed such selective compression of the bright-dark axis using a task where subjects matched tests in a pre-adapted region to ones in an un-adapted region. Tests were bright or dark pinstripes on a gray background, and pre-exposure was to multiple drifting pinstripes. Matches made after pre-exposure indicate a combination of symmetric and asymmetric compression, with more compression when adapting and test stimulus were similar in contrast polarity.
Light-adapted foveal luminance increment thresholds were measured for white photopic targets of 1.5-arc min diameter and 220-ms duration. We aimed to learn about the properties of mechanisms that subserve the detection of these targets. To study this subject we developed a noise probe technique that inserts noise close to the site of the stimulus. Threshold is more than doubled when zero-mean luminance noise is placed at a pair of flanking spots in the horizontal meridian centered on the test spot and 1.5 arc min distant. The detection mechanisms thus has a broad field, since noise effects persist at 5-arc min separation. The masking effect increases when the noise is in antiphase at the two flanking spots. Neither even- nor odd-symmetric mechanisms are able to explain these findings, regardless of whether linear or nonlinear processing is employed. The target detection may be mediated in part by a motion-sensitive mechanism.
Three red/green blind observers (dichromats) performed a wavelength discrimination task over a wide range of intensity levels. As expected, discrimination failed in the entire red/green spectral range at the low intensities typically used in wavelength discrimination experiments, but at very high intensities (at or above 10,000 td) discrimination was well maintained into the red/green range. The following experiments demonstrate that dichromats are able to utilize signals from the blue-sensitive cones (S-cones) to mediate color discrimination throughout the spectrum at high intensities, and they provide an estimate of S-cone sensitivity throughout the visible spectrum.
When an high frequency grating of high retinal contrast is presented intermittently by modulating its contrast at constant average luminance, observers experience uniform field flicker, even if the grating is too fine to be resolved. For long and middle wavelength cones, this contrast-modulation flicker can be seen for fringe periods as small as the diameter of a cone [MacLeod & He (1993). Nature, 361, 256-258], implying no substantial neural spatial integration prior to the nonlinear site. We now report that the short-wavelength cone system, despite its greater spatial integration than the other cone systems, can generate contrast-modulation flicker at spatial frequencies as high as 50 cycles/deg, a value comparable with that of the other cone systems in the same retinal area. Spatial resolution at the nonlinear site is in all cases apparently limited by the size of the cones. Likewise, little temporal filtering (in the range up to 18 Hz) precedes the S-cone nonlinearity. This suggests that the reduced S-cone system sensitivity for rapid flicker is due to postreceptoral limitations.
BACKGROUND: The perceived color at each point in a visual scene depends on the relationship between light signals from that point, and light signals from surrounding areas of the scene. In the well known phenomenon of simultaneous color contrast, changing the overall brightness or hue of an object's surround induces a complementary shift in the perceived brightness or hue of the object's color. Color contrast is thought to contribute to color constancy with changes in illumination. RESULTS: We report a new type of simultaneous color contrast, in which changing only the variance (i.e. contrasts and saturations), but not the mean, of colors in a test spot's surround induces a complementary shift in the perceived contrast and saturation of the test spot's color. Objects appear much more vivid and richly colored against low-contrast, gray surrounds than against high-contrast, multicolored surrounds. CONCLUSIONS: Color appearance depends not just on the mean color of the surround, but also on the distribution of surround colors about the mean. This novel form of simultaneous color contrast is inconsistent with a variety of models of color appearance, including those based on sensitivity regulation at the receptor level, and those in which the effects of complex surrounds on color appearance can be reduced to adaptation to the illuminant or induction from a homogeneous 'equivalent surround'. It tends to normalize the gamut of perceived colors in each visual scene and may also contribute to color constancy under viewing conditions that affect contrast.
How are binocular disparities encoded and represented in the human visual system? An 'encoding cube' diagram is introduced to visualise differences between competing models. To distinguish the models experimentally, the depth-increment-detection function (discriminating disparity d from d +/- delta d) was measured as a function of standing disparity (d) with spatially filtered random-dot stereograms of different centre spatial frequencies. Stereothresholds degraded more quickly as standing disparity was increased with stimuli defined by high rather than low centre spatial frequency. This is consistent with a close correlation between the spatial scale of detection mechanisms and the disparities they process. It is shown that a simple model, where discrimination is limited by the noisy ratio of outputs of three disparity-selective mechanisms at each spatial scale, can account for the data. It is not necessary to invoke a population code for disparity to model the depth-increment-detection function. This type of encoding scheme implies insensitivity to large interocular phase differences. Might the system have developed a strategy to disambiguate or shift the matches made at fine scales with those made at the coarse scales at large standing disparities? In agreement with Rohaly and Wilson, no evidence was found that this is so. Such a scheme would predict that stereothresholds determined with targets composed of compounds of high and low frequency should be superior to those of either component alone. Although a small stereoacuity benefit was found at small disparities, the more striking result was that stereothresholds for compound-frequency targets were actually degraded at large standing disparities. The results argue against neural shifting of the matching range of fine scales by coarse-scale matches posited by certain stereo models.
It is widely held that in human spatial vision the visual scene is initially processed through visual filters, each of which is responsive to narrow ranges of image spatial frequencies. The physiological basis of these filters are thought to be cortical neurons with receptive fields of different sizes. The grain of the neural representation of spatial vision is much finer than had been supposed. Using laser interferometry, which effectively bypasses the demodulation of the optics of the eye, we measured discrimination of, and adaptation to, high spatial frequency laser interference fringe patterns. Spatial frequency discrimination was good right up to the visual resolution limit (average Weber fractions of 0.13 at 50 c/deg). Both contrast and spatial frequency matches made after adapting to extremely fine interference fringes strongly suggested that there existed even finer, relatively unadapted, filters (mechanisms with small receptive fields). The smallest cortical receptive fields processing spatial information in human vision are so small that they can possess receptive field centers hardly wider than single cone photoreceptors.
Contrast sensitivity for orientation discrimination is limited to spatial frequencies below 50-60 cycles per degree by neural spatial integration, and we find that contrast sensitivity, measured using an orientation-discrimination criterion, declines sharply with increasing spatial frequencies in that range. Yet interference fringe patterns pulsed at constant mean luminance can be detected at spatial frequencies far above that resolution limit [D.R. Williams, Vision Res. 25, 195 (1985)]. This is due at least in part to aliasing by the receptor mosaic, but another possible cue is provided by nonlinear distortion, which can create spatially uniform temporal transients when a pulsed fringe pattern is presented. We investigated the contribution of these spatially unstructured distortion products to grating detection by superimposing the pulsed fringe patterns on a randomly flickering uniform field. This manipulation has almost no effect on contrast sensitivity well below the resolution limit. Just above the resolution limit, however, the random luminance mask greatly elevates the fringe pattern detection threshold, suggesting that spatially unstructured cues provide the basis for detection in this range. At still higher fringe pattern frequencies, which approximately match the cone mosaic, the random luminance flicker again becomes ineffective for some observers, creating a clear secondary peak in contrast sensitivity in the flicker mask condition, which is presumably due to spatially structured cues provided by aliasing with the cone mosaic. The aliasing peak is still more clearly demarcated if the subject sets contrast thresholds for the perception of pattern as such. The contrast sensitivity function then has a notch or gap between the normal sensitivity range and the aliasing range. Apparently, in the unmasked case, spatially uniform cues (changes in overall color and brightness) bridge this gap.
Contrast thresholds for 75% correct depth identification in narrow-band filtered random dot stereograms were determined for different center spatial frequencies and binocular disparities. Rigorous control over vergence was maintained during testing, and a forced-choice procedure was used. The resulting contrast sensitivity function for stereopsis revealed sensitivity over a greater range of disparities at low than at high spatial frequencies. Sensitivity peaked for large disparities at low spatial frequencies and for small disparities at high spatial frequencies. When disparities were converted to effective binocular phase differences, the variation of contrast sensitivity with phase followed a consistent pattern across spatial frequencies, with peak sensitivity occurring mainly for binocular phases of between 90 degrees and 180 degrees. These results have implications for the extent of spatial integration at the input to the disparity sensing mechanism. A model postulating a spread of positional disparities independent of the spatial frequency selectivity of disparity-sensitive units cannot account for the results. But the size-disparity correlation strongly evident in our data is predicted by certain models of stereopsis, such as phase disparity encoding. An ideal observer analysis is developed that demonstrates that our results were not forced by the nature of the stimulus employed; rather, the quantum efficiency for stereopsis at contrast threshold follows the size-disparity correlation.
Using a laser interferometer we can create grating patterns of high optical contrast (interference fringes) directly on the retina. With coarse fringe patterns, the alternating light and dark bars of the pattern can be seen, but the bars of the finest fringes are not subjectively resolved. We report here that when we rapidly modulate the contrast of a fine fringe pattern (keeping overall luminance constant), observers experience flicker, even if the fringes are too finely spaced to be perceived as a grating. For this flicker to be seen, the pattern needs to be resolvable by the photoreceptors themselves, but not necessarily by later stages of visual processing. It can be explained if, in man, signals associated with individual cone receptors do not depend linearly on light intensity, but instead are scaled by a fast sensitivity-regulating or light-adaptation mechanism. Contrast-modulation flicker is not demonstrable in rod vision; rod vision therefore lacks such a local adaptation process.
We present evidence that adaptation occurs in the separate links that connect the receptors to the luminance and the chromatic channels. The relative effectiveness of the L and M cone inputs to the luminance and red/green chromatic channels was determined by using, respectively, heterochromatic flicker photometry and a cancellation technique which maintained a pure yellow. The findings provide evidence for a link-specific adaptation model, wherein one receptor system provides two separate links to the luminance and chromatic channels and the outputs of an individual cone to these two postreceptoral channels can be separately attenuated or weighted at each of these links by colored adapting lights. One line of evidence for link-specific adaptation is that colored adapting fields selectively suppress L and M cone inputs to the red/green chromatic channel by a smaller factor than the luminance channel. A second line of evidence is that there is not only a magnitude difference but also a dynamic difference between adaptive processes operating in the luminance and chromatic channels: the luminance channel has a faster gain change and recovery from adaptation than does the chromatic channel. The results, together with other evidence, make it plausible that an important component of light adaptation in cone vision occurs at the cone-bipolar synapse.
Flickering lights that are detected by the blue cones of the human visual system fuse to yield a steady sensation at much lower rates of flicker than do lights that are detected by the red or green cones. Yet, although blue-cone-detected lights flickering at 30-40 Hz appear to be steady, they are still able to interact with red- or green-cone-detected flickering lights to produce clearly detectable beats in the form of an amplitude modulation of the red- or green-cone flicker. Thus the blue cones produce a viable high-frequency flicker signal, as do the red and green cones, but one that is normally lost before it reaches sensation. The temporal-frequency response for the blue-cone beat interaction is similar in shape to the temporal-frequency response for directly detected red- or green-cone flicker. When measured through the same pathway (which we identify as the luminance pathway, since it is able to transmit high-frequency flicker), the response of the blue cones seems to be as fast as that of the other cones.
Spectral sensitivity in the red-green spectral range typically reflects the joint influence of the middle-wavelength-sensitive cones (the M or green cones) and long-wavelength-sensitive cones (the L or red cones). The balance of M- and L-cone influence can be altered by presenting the test lights superimposed upon steady background fields of long or short wavelength. We find that presenting test stimuli just after an abrupt exchange between two colored backgrounds permits an easier and closer approach to cone isolation than presenting them either on a steady background or following an intense bleach. Background exchange drives the flicker detection or flicker photometric spectral sensitivities measured at 17 Hz to a limiting condition at lower intensities than do steady backgrounds. This condition is consistent with either M- or L-cone isolation. Steady backgrounds do not produce complete cone isolation: even on backgrounds that push spectral sensitivity closest to M or L, there are substantial phase differences between flickering lights of different color. In contrast, no phase differences remain following background exchange. The improvement in cone isolation produced by the exchange procedure is not confined to flicker measurements: the spectral range over which subjects are temporarily monochromatic is more extended following background exchange than on steady fields.