Human Fovea Research Articles

On-line feedback control of human visually guided slow ramp tracking: effects of spatial separation of visual cues

Visual feedback control of tracking movements is dependent upon a visual comparison of the guiding target and moving limb positions but the human fovea greatly restricts the area of high acuity vision. The effect of vertically separating the target and movement cues in a slow movement task is investigated. Subjects track a slow constant velocity target in the horizontal plane with wrist flexion controlled cursor movements. The effects of changes in the vertical distance between the two cues upon tracking performance were observed. When both cursors were at the same level, tracking was most accurate but showed significant intermittency around 2 Hz in frequency. Increased separation of cues reduced significantly both accuracy and intermittency; tracking was smoother but less accurate. Thus, feedback control is dependent upon the efficiency of positional comparison and hence becomes less effective as the cue separation increases. These results also support previous studies suggesting each cue makes an equal contribution to visuomotor feedback control, each acting as a reference to the other.

Electrical Coupling between Mammalian Cones

Background: Cone photoreceptors are noisy because of random fluctuations of photon absorption, signaling molecules, and ion channels. However, each cone's noise is independent of the others, whereas their signals are partially shared. Therefore, electrically coupling the synaptic terminals prior to forward transmission and subsequent nonlinear processing can appreciably reduce noise relative to the signal. This signal-processing strategy has been demonstrated in lower vertebrates with rather coarse vision, but its occurrence in mammals with fine acuity has been doubted (even though gap junctions are present) because coupling would blur the neural image.Results: In ground squirrel retina, whose triangular cone lattice resembles the human fovea, paired electrical recordings from adjacent cones demonstrated electrical coupling with an average conductance of approximately 320 pS. Blur caused by this degree of coupling had a space constant of approximately 0.5 cone diameters. Psychophysical measurements employing laser interferometry to bypass the eye's optics suggest that human foveal cones experience a similar degree of neural blur and that it is invariant with light intensity. This neural blur is narrower than the eye's optical blur, and we calculate that it should improve the signal-to-noise ratio at the cone terminal by about 77%.Conclusions: We conclude that the gap junctions observed between mammalian cones, including those in the human fovea, represent genuine electrical coupling. Because the space constant of the resulting neural blur is less than that of the optical blur, the signal-to-noise ratio can be markedly improved before the nonlinear stages with little compromise to visual acuity.

Photoreceptor inner segments in monkey and human retina: mitochondrial density, optics, and regional variation.

The present work quantifies aspects of photoreceptor structure related to mitochondria, inner segment dimensions, and optical properties, as a basis for furthering our understanding of rod and cone function. Electron-microscopic analyses were performed on the retina of one stumptail macaque (Macaca arctoides) to obtain stereological measurements of ellipsoid mitochondrial density, and sizes and shapes of outer and inner segments. In addition, the distribution of mitochondria and the optical properties of human foveal cones were examined with electron microscopy and Nomarski differential interference contrast (NDIC) imaging. Mitochondria comprised 74-85% of cone ellipsoids and 54-66% of rod ellipsoids in macaque. Ellipsoid volume increased with eccentricity by 2.4-fold for rods and more than 6-fold for cones over eccentricities to 12.75 mm, while the volume of the outer segment supported by the ellipsoid was essentially constant for both rods and cones. Per unit volume of outer segment, cones contained ten times as much mitochondria as rods. In human fovea, as in the rest of the retina, most cone mitochondria were located in the distal inner segment. In the foveal center, however, there are also mitochondria in the myoid, as well as in the outer fiber, proximal to the external limiting membrane (ELM). Analyses of the optical aperture of human foveal cones, the point at which their refractive index clearly differs from the extrareceptoral space, showed that it correlated well with the location of mitochondria, except in the foveal center, where the aperture appeared proximal to the ELM. While mitochondria have an important metabolic function, we suggest that the striking differences between rods and cones in mitochondrial content are unlikely to be determined by metabolic demand alone. The numerous cone mitochondria may enhance the waveguide properties of cones, particularly in the periphery.

Relative number of long- and middle-wavelength-sensitive cones in the human fovea.

Flicker photometric measurements yield spectral sensitivity curves that are well fitted by sums of the spectral sensitivity curves of long-wavelength-sensitive (L) cones and middle-wavelength-sensitive (M) cones if the L cones are given twice the weight of the M cones. This result has been interpreted as implying that L cones are more numerous than M cones but is also consistent with a different numerical ratio, say, 1:1, and with the assignment of greater weight to the L cone input than to the M cone input by the mechanism subserving flicker photometry. Measurements of temporal sensitivity are presented for lights that modulate the inputs of either only the L cones or only the M cones. Sensitivity to modulation of the L cones is approximately twice that of modulation of the M cones at approximately 30 Hz, but that advantage disappears at approximately 2 Hz. Thus flicker sensitivity is equivocal with regard to cone numerosity. Electrophysiological, anatomical, and psychophysical evidence is reviewed, with particular weight placed on the statistics of color appearance of small, brief, monochromatic lights and on increment thresholds measured on the same observers. It is concluded that, in the central fovea, the ratio of L:M cone numbers is close to unity and may not be so variable as is usually supposed.

A journey in color space

The idea that the first stage in normal daylight vision is characterized by three processes having different spectral sensitivities was established early in the 19th century by Young1 and linked clearly to experimental data on color matching by Maxwell.2 Hering's3 notion of opponent processes was grounded in facts of color appearance. A number of “opponent process” theories were developed to account for color appearance, in which the signals from the receptors were combined to form two channels conveying chromatic information and a third carrying achromatic information.4 More recently psychophysical, as opposed to phenomenological, evidence has been advanced in support of the existence of opponent mechanisms.5–12 While these articles provided evidence for the interaction of cone signals, they did not determine in detail the weights of the contributions of the different classes of cones to the second stage (and higher-order) mechanisms. The work discussed here was intended to determine the weights of the second-stage mechanisms by psychophysical means.13 Quantitative reanalysis of the results of habituation experiments demonstrated the existence of higher-order mechanisms that respond to the sums of the signals from second-stage mechanisms.14 Diverse evidence from other psychophysical experiments including detection and discrimination of chromatic pulses,14 and coherence of plaid patterns,15 confirmed the existence of higher-order mechanisms. Single unit recording from striate cortex in monkey revealed cells having the spectral sensitivities implied by the psychophysical results.16 Electrical recording of responses in monkey lateral geniculate nucleus (LGN) revealed single units with weights corresponding to the cardinal directions psychophysically determined.17 LGN cells show no sign of fatigue but units in V1 do.18 They also exhibit the wide range of spectral sensitivities required of higher-order mechanisms. Studies of the influence of the chromatic content of stimuli on vernier acuity and motion thresholds and on temporal modulation sensitivity support the conjecture that, while chromatic stimuli are processed solely by the parvocellular system, luminance stimuli are processed by both magno- and parvocellular neurons. The variation of the relative sensitivity of the L and M cones with temporal frequency, together with analysis of the statistics of color appearance of small, brief, near threshold monochromatic stimuli and data from Stiles's increment threshold experiment19 suggest that the numerosity ratio of L:M cones in the normal human fovea is more likely to be 1:1 than 2:1. © 2000 John Wiley & Sons, Inc. Col Res Appl, 26, S2–S11, 2001

Distribution and development of short‐wavelength cones differ between Macaca monkey and human fovea

Distribution and development of short‐wavelength cones differ between Macaca monkey and human fovea

A high-density differential screening strategy for identification of fovea genes with altered expression in the retina during aging

A human fovea cDNA library was arrayed at high-density and reacted with age-specific (4 yr & 80 yr) retinal probes to identify genes with altered expression during aging. Using this approach, we screened 55,368 genes by Southern analysis and determined that ∼0.7% are differentially expressed in young and old tissues. Northern analysis of total RNA from retina of humans aged 2–94 yr show that expression of one of the clones identified (clone dd112) decreases with aging.

Distribution and development of short-wavelength cones differ betweenMacaca monkey and human fovea

Macaca monkey and humans have three cone types containing either long-wavelength (L), medium-wavelength (M), or short-wavelength (S)-specific opsin. The highest cone density is found in the fovea, which mediates high visual acuity. Most studies agree that the adult human fovea has a small S cone-free area, but data are conflicting concerning S-cone numbers in the adult Macaca monkey fovea, and little evidence exists for how either primate fovea develops its characteristic cone pattern. Single- and double-label in situ hybridization and immunocytochemistry have been used to determine the pattern of foveal S cones in both the fetal and adult Macaca and human. Both labels find a clear difference at all ages between monkey and human. Adult humans have a distinct but variable central zone about 100 microm wide that lacks S cones and is surrounded by a ring in which the S-cone density is 8%. This S cone-free zone is detectable at fetal week 15.5 (Fwk15.5), shortly after S opsin is expressed, and is similar to the adult by Fwk20.5. Adult monkey foveas have an overall S-cone foveal density of 10%, with several areas lacking a few S cones that are not coincident with the area of highest cone density. A surrounding zone at 200-microm eccentricity has an S-cone density averaging 25%, but, by 800 microm, this has decreased to 11%. Fetal day 77-135 monkeys all have a distribution and density of foveal S cones similar to adults, although the high-density ring is not obvious in fetal retinas. Estimates of the numbers of S cones missing in the fetal human fovea range from 234 to 328, whereas no more than 40 are missing in the fetal monkey. These results show that, in these two trichromatic primates, S-cone distribution and the developmental mechanisms determining S-cone topography are markedly different from the time that S cones are first detected.

Determination of the foveal cone spacing by ocular speckle interferometry: limiting factors and acuity predictions.

We have developed a high-resolution imaging technique, based on speckle interferometry, for the objective determination of the cone spacing in the living human fovea. The spatial resolution attained with this technique is theoretically diffraction limited by the pupil size. However, the highest frequency that we measure varies greatly among subjects, especially for fully dilated pupils. We have conducted several experiments (determination of the cutoff frequency of ocular speckle interferometry, the double-pass modulation transfer function, and the Stiles-Crawford effect) that indicate that, as expected, the resolution is not limited by the incoherent modulation transfer function. We found, though, a high correlation between the cutoff frequency and the width of the eye's Stiles-Crawford function. This implies that the resolution depends on the structural properties of the cone mosaic itself. In addition, we have compared the Nyquist frequency of the cone mosaic, determined objectively by our technique, with the grating visual acuity measured in the same eyes at the same foveal eccentricities. For our subjects, visual resolution nearly matches the Nyquist frequency within the fovea, except at the foveal center, where the optical transfer function of the eye attenuates the contrast of frequencies close to the Nyquist limit to a value below threshold.

Color Perception of Aperture Colors Using a Computational Model of the Human Visual System

A previously developed model of the human fovea is modified for the analysis of colored stimuli. Whenever possible human and other primate anatomical, electrophysiological, and psychophysical data are incorporated into the computational model. Channels carrying information about color are represented by the summed responses of midget C- and L-type cells. The spectral energy distribution of any colored stimulus produces within the cell types a unique pattern of activities from which the amounts of each of the HUES (i.e., RED, GREEN, BLUE, and YELLOW), WHITENESS, BRIGHTNESS, and SATURATION can be determined. The present analysis is restricted to the fovea, where color vision is optimal and rods are absent or minimal. Psychophysical and model data are in good agreement as to the three attributes of aperture colors i.e., HUE, BRIGHTNESS, and SATURATION. As a result of univariance, information as to the spectral distribution of the stimulus cannot be used, and this creates a problem as to how to normalize colored stimuli to a common set of standards. A method based on normalization of the outputs of the retinal cells to a common WHITE is presented.

Classifying illusory contours: edges defined by "pacman" and monocular tokens.

Thresholds for the discrimination of orientation were measured in the human fovea for figures and borders delineated by solid lines and by "pacman" tokens as introduced by Kanizsa, as well as by contours induced by monocular tokens giving a stereoscopic depth illusion of a knife edge. Orientation discrimination of these illusory contours is poorer by a factor of approximately 2 than that of equivalent contours made of solid lines and is not much better than that for their supporting structures if taken alone. It is concluded that these kinds of illusory borders do not address the "border" or "edge" mechanism in the same way as real lines. Orientation discrimination and simultaneous orientation contrast (tilt illusion) were compared for a variety of illusory borders. The more robust the borders, i.e., the more sensitive to changes in orientation, the less their susceptibility to the tilt illusion.

Coherent imaging of the cone mosaic in the living human eye

A new system for the recording of high-resolution images of the cone mosaic in the living room fovea has been developed. The experimental method is inspired by stellar speckle interferometry, used in astronomy to resolve binary stars. Series of short-exposure images of small areas of the fovea are registered under coherent illumination. These images show speckle patterns that have some correlation with the topography of the cone mosaic and retain high-resolution information. Such correlation is better revealed in the power spectrum (square modulus of the Fourier transform). The signal-to-noise ratio is increased, without loss of high frequencies, by averaging the power spectra of a number of such speckle patterns. The average power spectra show, in most of the cases, an elliptical ring (or hexagon), whose mean radius corresponds to the characteristic spatial frequency of the cone mosaic (or the inverse of the mean row-to-row cone spacing) at a given retinal location. Good results are obtained in the five normal observers tested, at various retinal eccentricities, up to 1 visual degree, including the center of the fovea for two eyes. We find a decrease in the spatial frequency of the mosaic with the eccentricity and an important intersubject variability, in agreement with anatomical studies.

Characterization of a Human Fovea cDNA Library and Regional Differential Gene Expression in the Human Retina

The primate fovea is the region of the retina responsible for acute vision. This region constitutes less than 5% of the total area of the retina and has not been intensely studied at the molecular level. As a first step in the molecular characterization of the fovea, we have constructed a primary human fovea cDNA library. Experiments confirm that our cDNA library reflects a nonbiased distribution of foveal expressed sequences. Single-pass sequencing was performed on 209 randomly isolated clones from this library. Analysis of the sequences generated reveals that the distributions of fovea clones with either human mitochondrial gene sequences or repetitive elements are different than those observed in cDNA libraries made from other tissues. A significant number of the fovea expressed sequence tags (ESTs) (88, 42.1%) represent novel human ESTs. This suggests that the library will be useful in identifying new human genes. Northern analysis of specific fovea ESTs defined in this study suggests that there are significant quantitative differences in gene expression that distinguish the fovea from the rest of the retina.

Rank orderings of photoreceptor photon catches from natural objects are nearly illuminant-invariant

To examine the potential contribution of first-stage photoreceptor adaptation to color constancy, photon catches from 337 natural objects illuminated with phases of daylight and tungsten light were calculated for a model human fovea. The rank ordering of these photon catches within each cone photoreceptor class was examined. When first-stage adaptation is modeled using multiplicative or subtractive mechanisms, or a monotonic nonlinearity, no reordering of the rank ordering of photon catches is possible across illuminant changes. The observed rank orderings remained nearly invariant across illuminant changes for all three photoreceptor classes, although there was some local shifting in the rank orderings, thus ruling out the ability of von Kries adaptation alone to produce perfect color constancy. This means that for objects with natural reflectance spectra, the ordinal relationships between the photon catches within a class of photoreceptors exhibit only minor changes for these illuminant shifts. This result may be attributable to the fact that approx. 95% of the variance in these reflectance spectra is captured by the first principal component; objects that produce relatively few absorptions under one phase of daylight illumination will also produce relatively few absorptions under another phase. A geometric formalism for understanding these relationships is presented, and limitations on this analysis are discussed.

The spatial arrangement of cones in the primate fovea.

The retinae of Old World primates contain three classes of light-sensitive cone, which exhibit peak absorption in different spectral regions. But how are the different types of cone arranged in the hexagonal mosaic of the fovea? This question has often been answered with artists' impressions, but never with direct measurements. Staining for antibodies specific to the short-wave photopigment has revealed a sparse, semiregular array of cones; but nothing is known about the arrangement of the more numerous long- and middle-wave cones. Are they randomly distributed, with chance aggregations of one type, as Hartridge postulated in these columns nearly 50 years ago? Or do they exhibit a regular alteration, recalling the systematic mosaics seen in some non-mammalian species? Or, conversely, is there positive clumping of particular cone types, as might be expected if local patches of cones were descended from a single precursor cell? We have made direct microspectrophotometric measurements of patches of foveal retina from Old World monkeys, and report here that the distribution of long- and middle-wave cones is locally random. These two cone types are present in almost equal numbers, and not in the ratio of 2:1 that has been postulated for the human fovea.

Hand-eye coordination during sequential tasks.

The small angle subtended by the human fovea places a premium on the ability to quickly and accurately direct the gaze to targets of interest. Thus the resultant saccadic eye fixations are a very instructive behaviour, revealing much about the underlying cognitive mechanisms that guide them. Of particular interest are the eye fixations used in hand-eye coordination. Such coordination has been extensively studied for single movements from a source location to a target location. In contrast, we have studied multiple fixations where the sources and targets are a function of a task and chosen dynamically by the subject according to task requirements. The task chosen is a copying task: subjects must copy a figure made up of contiguous coloured blocks as fast as possible. The main observation is that although eye fixations are used for the terminal phase of hand movements, they are used for other tasks before and after that phase. The analysis of the spatial and temporal details of these fixations suggests that the underlying decision process that moves the eyes leaves key decisions until just before they are required.

Simultaneous measurement of two-point-spread functions at different locations across the human fovea

An experimental system for measuring simultaneously the retinal images of two-point tests has been developed. In particular we present one experiment in which one of the points is located at the center of the fovea and the other one is at 1 deg of eccentricity. At these two foveal locations the optical image quality is expected to be approximately the same, while the structure of the retina is known to be quite different. Our results of aerial images show small but systematic differences between the two-pointspread functions that are measured at 0 and 1 deg of eccentricity. The image quality is always slightly better in the center of the fovea with the differences more marked in the nasal and inferior orientations. That could be explained by a small but noticeable contribution of the retinal thickness to the optical aberrations of the eye. The possible increment of scattering caused by the increase in retinal thickness at 1 deg was barely measurable in our experiment. An indirect consequence is that retinal reflection has little practical influence on our particular double-pass measurements of the eye's image quality.

A morphological comparison of foveal development in man and monkey

The fovea can first be identified in both monkey and human retina at 26-30% gestation as a region containing all adult retinal layers and only cone photoreceptors. A shallow foveal pit and cone outer segments appear by 63-65% gestation in both species. Prenatal development continues rapidly in the monkey, so that by birth a single layer of inner retinal neurons are present in the fovea, cones are three cells deep, inner segments are elongated, and outer segments are up to 50% of inner segment length. In contrast, human fovea does not reach a similar stage until several months after birth. The fovea is adult-like in monkey at 12 weeks and in human at 11-15 months, although human will mature further up to four to five years. This study shows that human fovea is less mature at birth than monkey but develops rapidly in infancy, suggesting that it may be even more susceptible to postnatal environmental influences than the commonly-used monkey model.

A simulated human fovea: the L-type cells of the magnocellular pathway

A static model of the human fovea is used to study the properties of L-type amacrine cells (L-AC) that link the cones with the magnocellular pathway. Sine and square wave gratings are used to obtain response spectra of L-ACs and C-type bipolar cells (C-BC); these two types of cells are compared in both central fovea, where there are no blue-sensitive cones and parafovea, where the blue-sensitive cones 12% of the population. Three dispersion conditions are used: no, aberration-free, and chromatic dispersions. The abilities of L- and C-type cells to resolve a two-bar image are also compared. The findings are consistent with the magnocellular pathway having higher contrast luminance and chromatic sensitivity gains than those of the parvocellular pathways, but under specified conditions. And under specified conditions the findings are also consistent with both pathways being involved in the detection of chromatic and achromatic signals. Nevertheless when all factors are considered the parvocellular pathway appears to be involved with fine spatial and chromatic tuning while the magnocellular pathway appears to deal with coarser tuning.

Simulated bipolar cells in fovea of human retina

The ability of simulated bipolar cells (BC) of the human central fovea to resolve images is studied with a two-bar stimulus using a resolution index (RI) as a measure of resolvability. RIs are determined for intensity and chromatic contrasts using all combinations of white, black, red, yellow, green, and blue lights. Various cone matrixes and BC receptive field organizations are studied for orientation preference by using two-bars oriented either 0, 45, 90, or 135 degrees to the horizontal axis of the retina. Nonpreference for orientation, i.e. RI does not change with bar orientation, varies with matrix type, and receptive field organization. For a given orientation RI increase asymptotically as bar width or length, or gap between the bars increases. Systematic changes in RI occur with systematic changes in contrast. For most color pairs there are residual RIs at isoluminance.