Nasotemporal Asymmetry Research Articles

Latent Fixation Nystagmus and Nasotemporal Asymmetries of Motion Visually Evoked Potentials in Naturally Strabismic Primate

To determine whether macaque monkeys who had onset of natural, alternating esotropia in early infancy have the eye movement abnormalities and motion visually evoked potential (VEP) abnormalities observed in human infantile esotropes. Recordings were obtained of horizontal pursuit eye movements and fixation nystagmus under conditions of monocular viewing. Motion VEPs in response to horizontal motion were recorded with the animals sedated to reduce the possibility of eye movement artifact. The strabismic monkeys had a naso-temporal asymmetry of horizontal pursuit favoring nasally directed motion when viewing with either eye. When fixating stationary targets, latent nystagmus was apparent; the eyes drifted conjugately and the slow phase of the nystagmus was always nasally directed with respect to the fixating eye. Motion VEPs were characterized by a strong horizontal asymmetry with the directional bias inverted approximately 180 deg in the two eyes. These eye movement and motion VEP asymmetries were not observed in a normal macaque. Macaque monkeys who have infantile esotropia possess asymmetries of horizontal pursuit and motion VEPs like those documented in strabismic humans. Macaques with infantile esotropia appear to be an appropriate animal model for study of neural mechanisms in strabismus.

Grating and flicker sensitivity in the near and far periphery: Naso-temporal asymmetries and binocular summation

A variety of recent physiological and psychophysical experiments provide evidence for a large asymmetry between nasal and temporal processing outside of the central 40° of visual field. Binocular processing has also been found to be reduced outside of this region even though the individual left and right eye fields continue to overlap for a full 120°. In an effort to help quantify these findings, monocular and binocular grating and flicker contrast sensitivities were measured in the fovea and in the near and far periphery. The results show a large asymmetry between nasal and temporal retinal grating sensitivity in the far periphery especially at high spatial frequencies. A smaller asymmetry was found for flicker but no differential effect of flicker frequency was found. The summation results are consistent with previous findings in showing greatly reduced binocular processing outside of the central 40°; this is especially true for the grating stimuli. These results are discussed with respect to possible physiological mechanisms. Peripheral

Dendritic competition in the developing retina: ganglion cell density gradients and laterally displaced dendrites.

Dendrites of retinal ganglion cells (RGCs) tend to be distributed preferentially toward areas of reduced RGC density. This, however, does not occur in the retina of normal pigmented rats, in which it has been suggested that the centro-peripheral gradient of RGC density is too shallow to provide directional guidance to growing dendrites. In this study, laterally displaced dendrites of RGCs retrogradely labeled with horseradish peroxidase were related to cell density gradients induced experimentally in the rat retina. Neonatal unilateral lesions of the optic tract produced retrograde degeneration of contralaterally projecting RGCs, but spared ipsilaterally projecting neurons in the same retina. These lesions created an anomalous temporal to nasal gradient of cell density across the decussation line, opposite to the nasal to temporal gradient found along the same axis in either normal rats or rats that had the contralateral eye removed at birth. RGCs in rats that received optic tract lesions had their dendrites displaced laterally toward the depleted nasal retina, while in either normal or enucleated rats there was no naso-temporal asymmetry. The lateral displacement affected both primary dendrites and higher-order branches. However, the gradient of cell density after optic tract lesions was less steep than the gradient in either normal or enucleated rats. To test for the presence of steeper gradients at early stages of development, RGC density gradients were also examined at postnatal day 5 (P5). In normal rats, the RGCs were homogeneously distributed throughout the retina, while rats given optic tract lesions at birth already showed a temporo-nasal density gradient at P5. Still, this anomalous gradient was less steep than that found in normal adults. It is concluded that the time course, rather than the steepness of the RGC density gradient, is the major determinant of the lateral displacement of dendritic arbors with respect to the soma in developing RGCs. The data are consistent with the idea that the overall shape of dendritic arbors depends in part on dendritic competition during retinal development.

Deviations from strict M scaling

It has been hypothesized that the visibility of stimuli can be made independent of location in the visual field if they are scaled according to the cortical magnification factor M (M scaling) [ Exp. Brain Res.37, 495 ( 1979); J. Opt. Soc. Am. A4, 1568 ( 1987)]. Although the predictions of this hypothesis are quite good with regard to contrast sensitivity for sine wave gratings, they are inaccurate with regard to the detection of circular disks: the visual field contains large regions where diameter-threshold curves for these stimuli are independent of retinal location [ Am. J. Optom.49, 748 ( 1970); Vision Res.20, 967 ( 1980)], although M varies by a factor of 3 over these regions. We measured diameter-threshold functions for circular symmetric stimuli with a Gaussian luminance profile and Gaussian temporal modulation at various eccentricities (as high as 42°) along both sides of the horizontal meridian. Along the temporal side the results are similar to those for disks: between 12° and 42° the curves are largely independent of eccentricity. In addition a strong nasotemporal asymmetry is found: for the nasal side the thresholds are considerably higher than for the temporal side. The results suggest both scale and gain differences over the visual field. Reanalysis of data for gratings shows that M scaling holds only for high spatial frequencies at which the slope of the contrast sensitivity function is steep (acuity); if the slope is less steep, the results are similar to those for localized stimuli. The results can be explained if we assume that (i) the spatial scale varies proportionally to the diameter of the smallest receptive field center and (ii) the gain is a function of the overlap factor, i.e., the number of retinal ganglion cells covering a single point in visual space.

Retinal growth in foveated teleosts: nasotemporal asymmetry keeps the fovea in temporal retina

Fish retinas continue to grow throughout life by adding neurons at the margin, with the result that cells born at a peripheral site are steadily displaced toward the center of the enlarging retina. This presents a functional problem for fish with specialized temporal areas such as a fovea--how to reconcile continual growth with the maintenance of a temporal location for the fovea. One possibility is that the retina grows asymmetrically, with most new retina added nasally, relatively little temporally. I have tested this hypothesis by evaluating retinal growth in marine teleosts from 15 families, both foveated and unfoveated. The pattern of growth was revealed by exploiting the fact that each new generation of ganglion cells sends its axons into the optic nerve as a cohort; small grains of the carbocyanine dye 1,1'-dioctadecyl-3,3,3',3'-tetramethyl-indocarbocyanine were applied to various sites in the cross section of the optic nerves of adults, and the retrogradely labeled cell bodies in the retina were visualized in whole-mounts. The labeled cells lay in annuli, each one a generation of ganglion cells. Representatives of seven of the families showed clearly asymmetric growth: the labeled annuli were close together on the temporal side and more distant nasally, the embryonic fissure curved from its ventral origin toward the temporal side, and in six of these families, labeled fibers from temporal retina skirted the fovea. Members of the other eight families, without specialized areas, had more symmetric retinal growth: labeled annuli were equally spaced on all sides, the embryonic fissure was vertical, and there were no skirting fibers. The following hypothesis is supported: the retina grows asymmetrically, and maintains the area for acute vision oriented toward the anterior field.

Psychophysical localization of the human visual streak.

In a topographical study of the human retina, Curcio and Allen documented the presence of the human visual streak, which they described as a prominent nasotemporal asymmetry in ganglion cell density. This asymmetry could also be expected to be measurable in any visual function limited by ganglion cell density. By using an interferometer we sought to test the hypothesis of Thibos et al. that peripheral resolution acuity is limited by the spacing of ganglion cells and should therefore reflect the anatomical asymmetry of the visual streak, once the attenuating effects of the eye's optics have been removed. This proved to be the case and differences predicted by a ganglion cell density of 2:1 were easily measurable. This study has potential clinical implications for the detection of disease or abnormalities of the visual system that cause death or dysfunction of retinal ganglion cells.

Human peripheral spatial resolution for achromatic and chromatic stimuli: limits imposed by optical and retinal factors.

1. The aim of this study was to determine whether optical, receptoral or higher-order neural properties limit spatial resolution (acuity) in human vision, especially in the peripheral regions of the visual field. 2. Both achromatic and chromatic stimuli were used, and measures were taken to ensure that the resolution estimates were not contaminated by the detection of spatial sampling artifacts. Spatial contrast sensitivity functions were measured at retinal locations from 0 to 55 deg along the naso-temporal meridian for: (i) discriminating the direction of drift of luminance-modulated (black-white) sinusoidal stimuli drifting at 8 Hz (achromatic task); and (ii) for detecting isoluminant red-green sinusoidal stimuli drifting at 0.4 Hz (chromatic task). Achromatic contrast sensitivity functions were also measured along the vertical meridian for eccentricities of 8 and 40 deg. Each achromatic function was extrapolated to a contrast sensitivity of one (100% contrast) to estimate achromatic acuity. Chromatic acuities were obtained by expressing chromatic contrast in terms of cone contrasts and using the same method of extrapolation. We compared the results with recent data on human optical properties and retinal anatomy. 3. Both achromatic and chromatic acuity decline with distance from the fovea, but at a faster rate than that dictated by the known optical and/or receptoral properties of the human eye. We conclude that, for stimuli of either achromatic or chromatic contrast, peripheral spatial resolution is limited by post-receptoral mechanisms. Also, chromatic acuity declines more steeply than luminance acuity with eccentricity suggesting that there are additional post-receptoral limitations on colour resolution in the periphery. 4. A clear naso-temporal asymmetry is seen in the resolution whose dependence is qualitatively, but not quantitatively, similar to the Nyquist limits imposed by the asymmetric density of human retinal ganglion cells. We discuss the possibility that in peripheral vision (beyond the optic nerve head) the spacing of ganglion cells may pose a fundamental limit on the resolution of achromatic stimuli, but not chromatic stimuli.

A perspective on psychophysical testing in children

In this paper, we show that the development of acuity in infancy is not due solely to foveal maturation, since there is a clear development of acuity in the peripheral visual field. The development of peripheral acuity, and the naso-temporal asymmetry during early development reinforce the idea that the visual loss in adult strabismic amblyopes is not due to an arrest of development, but rather to the chronic interocular suppression of the deviated eye. The Teller Acuity Card Test does not reliably detect strabismic amblyopia, and therefore should not be recommended as a screening test. However, the test is adequate for diagnosing visual losses in children with organic eye disorders and possibly anisometropia.

Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque) retina

Redistributions of monkey cones and rods during the first year after birth include a fivefold increase in peak foveal cone density from 43,000 to 210,000 cones/mm2, a decrease in the diameter of the rod-sparse area, and a two- to threefold decrease in peripheral photoreceptor density. Two weeks before birth, higher cone density is already apparent in the future fovea, as are the nasotemporal asymmetry in cone distribution, a higher density "cone streak" along the horizontal meridian, a large rod-sparse central fovea, and a ring of high rod density. Despite the early appearance of these basic patterns, photoreceptor distribution is not mature until 1 to 5 years postnatally. Total cones varied from 4 million at birth to 3.1 million in the average adult. The two oldest eyes had fewer cones, suggesting up to a 25% loss late in development. There were 60 to 70 million rods in the adult macaque retina and little evidence of postnatal changes in number. Neither of these small changes is sufficient to account for the reduction in peripheral photoreceptor density and both are in the wrong direction to explain increasing foveal density, ruling out a major role for either photoreceptor death or generation. Retinal area increased by a factor of 2.4 from 2 weeks before birth to adulthood. In contrast, the posterior pole of the retina was dimensionally stable throughout this period, with the distance between the fovea and optic disc varying nonsystematically from 3.37 to 4.05 mm. Retinal coverage of the globe was also stable at 48-60%. Thus postnatal growth can be ruled out as a factor in the density changes occurring in central retina. Adult retinas have a higher proportion of both cones and rods in midperiphery, whereas young retinas have a higher proportion of photoreceptors in far periphery. It appears that photoreceptors are radially redistributed from peripheral toward central retina during postnatal development, resulting in the marked increase in foveal cone density and the decrease in the eccentricity of the rod ring. Up to 13 weeks postnatally, midperipheral growth of the retina is substantial and increases with eccentricity. At later ages, expansion continues only in the very far periphery. Retinal growth appears sufficient to explain the decreases in peripheral rod and cone density with age. These and previous data strongly suggest that differentiated photoreceptors, with complex cytology and synaptic contacts, migrate toward the foveal center, explaining the increase in foveal photoreceptor density.(ABSTRACT TRUNCATED AT 400 WORDS)

Naso-temporal asymmetry of visual perception and of the visual cortex

The decrease of visual performance from the fovea towards the periphery depends upon the task tested. The slope of the decrease is generally steeper for hyperacuity than for spatial resolution and is steeper in the nasal than in the temporal hemifield. The naso-temporal asymmetry in the periphery of the visual field, beyond 20 deg eccentricity, is much more pronounced for hyperacuity than for spatial resolution. The psychophysical results show a close correlation to the cortical organization as revealed by autoradiography.

Limbal and axial chamber depth variations. A population study in Eskimos.

In an unselected population sample of 505 adult Greenland Eskimos limbal chamber depth (LCD) was estimated according to van Herick et al. (1969), and axial chamber depth (ACD) was measured optically using Haag Streit pachymetry. For comparison LCD was estimated in 308 Danes above 40 years. A marked naso-temporal asymmetry in LCD scoring was found indicating a shallower chamber at the temporal limbus. No corresponding gonioscopic asymmetry was observed. Significant age, sex, and ethnic variations were demonstrated, the lower levels of both parameters being found in elderly persons, women and Eskimos, respectively. Danes showed a lower level of LCD scores than reported in Americans. In detection of eyes showing shallow chambers in the Eskimo population (arbitrarily: ACD less than or equal to 2.0 mm) the van Herick slit-lamp test at temporal limbus yielded a sensitivity of 91%, a specificity of 53% and predictive values of a positive and a negative test of 30% and 96%, respectively. At gonioscopy narrow angles were often found among eyes showing LCD less than or equal to 1/4 of corneal thickness, even when ACD was greater than 2.0 mm (in 25%).