Intraocular pressure fluctuations of growing chick eyes are suppressed in constant light conditions.

We report measurements of intraocular pressure (IOP) in growing domestic chicks at 12 h intervals, with three different lighting conditions. One group of chicks was raised in 12 h light and 12 h darkness (N), another in constant light (CL), and the third group was initially exposed to CL for three weeks then returned to N for either one week or four weeks (CLN). Pressures were measured in the middle of the light and dark periods (noon and midnight) for N and CLN birds, and at corresponding 12 h intervals for CL birds (also noon and midnight). The IOP of N chicks fluctuated from a light period average value of 25 mm Hg ( ±1.3 SD), to a dark period average value of 17.5 mm Hg ( ±1.1 SD mm Hg; P < 0.0001). These pressures were established by 4 days of age. At 7 weeks, (N) IOP continued to fluctuate: light values were 21.7 mm Hg (±1.2 SD), and dark values were 18.3 mm Hg ( ±0.7 SD). The IOP of CL birds did not fluctuate, remaining steady at 17 mm Hg ( ±1.4 SD). Chicks exposed to CL for 3 weeks required more than one week in N to re-establish (N) IOP values. We conclude that IOP fluctuates in hatchling chicks under N light conditions, that fluctuation is suppressed in CL light conditions, and that IOP recovery from 3 weeks suppression in CL requires more than one week in N light conditions.

Plasticity in the growth of the chick eye: emmetropization achieved by alternate morphologies.

Both refractive properties of the eyes and ambient light conditions affect emmetropization during growth. Exposure to constant light flattens the cornea making chicks hyperopic. To discover whether and how growing chick eyes restore emmetropia after exposure to constant light (CL) for 3, 7, or 11weeks, we returned chicks to normal (N) conditions with 12h. of light alternating with 12h. of darkness (designated the "R", or recovery, condition) for total periods of 4, 7, 11, or 17weeks. The two control groups were raised in CL conditions or raised in N conditions for the same length of time. We measured anterior chamber depths and lens thicknesses with an A-scan ultrasound machine. We measured corneal curvatures with an eight-axis keratometer, and refractions with conventional retinoscopy. We estimated differences in optical powers of CL, R and N chicks of identical age by constructing ray-tracing models using the above measurements and age-adjusted normal lens curvatures. We also computed the sensitivity of focus for small perturbations of the above optical parameters. Full refractive recovery from CL effects always occurred. Hyperopic refractive errors were absent when R chicks were returned to N for as little as 1week after 3weeks CL treatment. In R chicks exposed to CL for 11weeks and returned to N, axial lengths, vitreous chamber depths and radii of corneal curvatures did not return to normal, although their refractions did. While R chicks can usually recover emmetropia, after long periods of exposure to CL, they cannot recover normal ocular morphology. Emmetropization following CL exposure is achieved primarily by adjusting the relationship between corneal curvature and axial length, resulting in normal refractions.

Lack of oblique astigmatism in the chicken eye.

Primate eyes display considerable oblique off-axis astigmatism which could provide information on the sign of defocus that is needed for emmetropization. The pattern of peripheral astigmatism is not known in the chicken eye, a common model of myopia. Peripheral astigmatism was mapped out over the horizontal visual field in three chickens, 43 days old, and in three near emmetropic human subjects, average age 34.7years, using infrared photoretinoscopy. There were no differences in astigmatism between humans and chickens in the central visual field (chicks -0.35D, humans -0.65D, n.s.) but large differences in the periphery (i.e. astigmatism at 40° in the temporal visual field: humans -4.21D, chicks -0.63D, p<0.001, unpaired t-test). The lack of peripheral astigmatism in chicks was not due to differences in corneal shape. Perhaps related to their superior peripheral optics, we found that chickens had excellent visual performance also in the far periphery. Using an automated optokinetic nystagmus paradigm, no difference was observed in spatial visual performance with vision restricted to either the central 67° of the visual field or to the periphery beyond 67°. Accommodation was elicited by stimuli presented far out in the visual field. Transscleral images of single infrared LEDs showed no sign of peripheral astigmatism. The chick may be the first terrestrial vertebrate described to lack oblique astigmatism. Since corneal shape cannot account for the difference in astigmatism in humans and chicks, it must trace back to the design of the crystalline lens. The lack of peripheral astigmatism in chicks also excludes a role in emmetropization.

Visual accommodation and active pursuit of prey underwater in a plunge-diving bird: the Australasian gannet.

Australasian gannets (Morus serrator), like many other seabird species, locate pelagic prey from the air and perform rapid plunge dives for their capture. Prey are captured underwater either in the momentum (M) phase of the dive while descending through the water column, or the wing flapping (WF) phase while moving, using the wings for propulsion. Detection of prey from the air is clearly visually guided, but it remains unknown whether plunge diving birds also use vision in the underwater phase of the dive. Here we address the question of whether gannets are capable of visually accommodating in the transition from aerial to aquatic vision, and analyse underwater video footage for evidence that gannets use vision in the aquatic phases of hunting. Photokeratometry and infrared video photorefraction revealed that, immediately upon submergence of the head, gannet eyes accommodate and overcome the loss of greater than 45 D (dioptres) of corneal refractive power which occurs in the transition between air and water. Analyses of underwater video showed the highest prey capture rates during WF phase when gannets actively pursue individual fish, a behaviour that very likely involves visual guidance, following the transition after the plunge dive's M phase. This is to our knowledge the first demonstration of the capacity for visual accommodation underwater in a plunge diving bird while capturing submerged prey detected from the air.

The effects of light regimes and hormones on corneal growth in vivo and in organ culture.

When chicks are exposed to constant light (CL) during growth, their corneas become flatter and lighter in weight, and their anterior segments become shallower than those of chicks exposed to cyclical periods of light and dark. These effects have been correlated with CL suppression of cyclical changes in melatonin levels. The question of whether light directly influences corneal growth (e.g. via cryptochromes in the cornea) or acts remotely via the suppression of the melatonin rhythm has not yet been answered. Retinoic acid (RA), an ubiquitous morphogen, also causes non-functional flattening during corneal growth, but its effect in vivo has not been correlated with light regimes. We wished to characterize and distinguish between hormonal and light effects on corneal growth. We used organ culture to study the direct effects of light regimes, melatonin, and RA, and compared these results with those of parallel in vivo experiments. In this study, eye drops containing melatonin or RA were applied to corneas exposed to CL in vivo or in organ culture, and effects on corneal mass and hydration were measured. We applied a melatonin blocker, luzindole, to chick corneas in normal light/dark conditions to confirm that the observed melatonin effects are mediated at the cell membrane. Anterior chamber depth and refraction in vivo were measured. We found that, during CL exposure, combined application of melatonin and RA eye drops increased the depth of the anterior segment in vivo, (P = 0.003) and interestingly, both also reduced the hyperopia of CL exposure after 2 weeks (P = 0.002), thus partially reversing the effects of CL. RA increased corneal hydration in vivo (P = 0.030) but not in organ culture. Melatonin had no effect on corneal hydration in vivo, but in organ culture, melatonin significantly decreased hydration (P < 0.001). We found no evidence for a direct effect of light on corneal hydration in growing chick corneas in culture. Melatonin is required for normal corneal growth in vivo, and together melatonin and RA, or RA alone, affects the regulation of water content within the chick cornea. Melatonin also affects corneal hydration in vitro, but RA does not.

Photorefraction of eyes: history and future prospects.

A brief history of photorefraction, i.e., the refraction of eyes by photography or computer image capture, is given. The method of photorefraction originated from an optical scheme for secret communication across the Berlin wall. This scheme used a lens whose focus about infinity was modulated by a movable reflecting surface. From this device, it was recognized that the vertebrate eye was such a reflector and that its double-pass pointspread could be used to compute its degree of defocus. Subsequently, a second, totally independent invention, more accurately termed "photoretinoscopy," used an eccentric light source and obtained retinoscopic-like images of the reflex in the pupil of the subject's eyes. Photoretinoscopy has become the preferred method of photorefraction and has been instantiated in a wide variety of devices used in vision screening and research. This has been greatly helped by the parallel development of computer and digital camera technology. It seems likely that photorefractive methods will continue to be refined and may eventually become ubiquitous in clinical practice.

Morphometrics of corneal growth in chicks raised in constant light.

In this study we wish to augment our understanding of the effect of environment on corneal growth and morphology. To understand how corneal development of chicks raised in constant light differs from that of 'normal' eyes exposed to cyclic periods of light and dark, white Leghorn chicks were raised under either constant light (approximately 700 lux at cage top) or in 12 h light/12 h dark conditions for up to 12 weeks after hatching. To determine whether corneal expansion is uniform, some birds from each group received corneal tattoos for periodic photographic assessment. By 16 days of age, constant light corneas weighed less than light/dark regimen corneas [7.39 +/- 0.35 mg (SE) vs. 8.47 mg +/- 0.26 mg SE wet weight, P < or = 0.05], and corresponding differences were seen in corneal dry weights. Spatial expansion of the corneal surface was uniform in both groups, but the rate of expansion was slower in constant light chicks [0.0327 +/- 0.009 (SE) vs. 0.144 +/- 0.018 (SE) mm(2) day(-1) for normal chicks, P < or = 0.001]. At 1 day of age, there were 422 +/- 12.5 (SE) stromal cells 0.01 mm(-2) in the central cornea and 393 +/- 21.5 (SE) stromal cells 0.01 mm(-2 )peripherally. Although this difference is not statistically significant, the cell densities in the central cornea were always larger than those of the peripheral cornea in all eight measurements over a 10.5-week period, and this difference is significant (P < or = 0.008, binomial test). Light/dark regimen birds show no such consistent difference in cell densities between central and peripheral corneas. Thus, the density distribution of corneal stromal cells of chicks grown in constant light differs from that of normal chicks. Taken together, all these observations suggest that diurnal cycles of light and darkness are necessary for normal corneal growth.

Role of the pineal gland in ocular development of the chick in normal and constant light conditions.

PURPOSE: To evaluate the role of the pineal gland in development of the chick eye in normal and constant light (CL) conditions. METHODS: Chicks (Gallus gallus) were raised in either a 12-hour light-dark cycle (12L/12D) or in CL, with or without opaque, removable hoods that covered the top of the head for 12 hours each day. An additional group was raised with opaque eye occluders over the right eye for 12 hours daily. Half of the chicks in each group had their pineal glands surgically removed at 3 to 6 days after hatching. Corneal curvature was measured with keratometry, anterior chamber depth with ultrasound, and refraction with infrared photoretinoscopy. RESULTS: Pinealectomy does not affect the development of the chick eyes either in 12L/12D or CL. Covering the right eyes provided the same amount protection against CL's effects on the corneal curvature of both eyes, with or without pinealectomy. Pinealectomized chicks were not protected from CL's effects by 12L/12D head covers. A similar pattern of responses was obtained for refraction and anterior chamber depth. CONCLUSIONS: Although 12L/12D covering of the pineal gland can protect chick eyes from CL's effects (corneal flattening, shallowing of the anterior chamber, and hyperopia), the pineal gland does not appear to be necessary for normal growth in 12L/12D conditions, and its absence does not affect eye growth in CL conditions, with or without hoods or occluders. Pinealectomy does not influence the protection of an eye exposed to CL that is afforded by covering the other eye in a 12L/12D cycle.

Changes in the refractive state during prey capture under low light in the nocturnal cardinalfish Apogon annularis.

Many nocturnal and crepuscular fish use vision to feed and function under low light levels. However, little is known about their ability to accommodate or their visual acuity under these light levels. We used Infrared Photoretinoscopy to track the refractive state of the eye during prey capture under low light in Apogon annularis, a nocturnal reef fish. Anatomical measurements of the eyes allowed calculations of visual acuity. Changes in the refractive state were observed in approximately 75% of the prey capturing strikes, preceding the strikes by 30 ms. These changes were rare between strikes or when prey was absent. Anatomical measurements indicated that the number of photo-detection units in a retinal image greatly exceeded the minimal number needed to detect prey. We conclude that nocturnal vision in A. annularis is sufficiently sensitive to allow accommodation during prey capture.

Growth of the cornea from infancy to adolescence.

The intraocular distance and iris diameter of children and young adolescents were measured, with the aid of a measuring microscope, from photographs of their faces. True intraocular distance was measured with an intraocular caliper at the same time that the photographs were taken. These data were then compiled and horizontal visible iris diameters (HVIDs) were calculated. An equation was derived from the optics of the Gullstrand model eye to calculate horizontal corneal diameter (HCD) from HVID. Comparisons of HVIDs revealed no significant correlation with age in either a regression plot of cross-sectional data for subjects aged 1 month to 1 year, or all subjects whose ages ranged from 1 month to adolescence. Additional longitudinal data for 13 individuals, who had been photographed as both an infant (mean = 3.4 months) and as an older child or adolescent (mean = 8.6 years), were then compiled and HVIDs for these subjects at two different ages were compared. A Wilcoxon signed rank test revealed a small but significant amount of growth, 0.318 mm (p-value = 0.013), in the HVIDs over a mean age difference of 8.3 years for individuals measured twice during their lifetimes. The regression equation for this growth was: HVID = 10.52 (+/-0.095 S.E.) + 0.0305 (+/-0.014) x Age (years). From a comparison of data from earlier literature and our own measurements, we conclude that, after birth, the fastest growth of the cornea must occur during the first few months of life.

Allometry and scaling of wave aberration of eyes.

The scaling of root mean square (RMS) wave aberration in an isometrically growing eye is investigated, along with changes due to measurements made at different relative pupil sizes. It is found that, relative to an initial state, if an eye expands in all directions by the factor k, and the wave aberration is then measured at a relative pupil size which has changed over the pupil size used for the original measurement by a factor b, the new wave aberration will be increased or decreased by a factor kb(n), where n is the exponent relating RMS wave aberration, to pupil radius, r, in the equation: RMS=qr(n) in the initial eye. This implies that, if wave aberration is measured in a growing eye with a constant measurement pupil size, the measured RMS will decrease by the factor 1/k(n-1).

Accommodative state of young adults using reading spectacles.

We examined the accommodative state of young adults wearing +2D and +3D reading spectacles under normal conditions and with the elimination of accommodative cues. Subjects' refractions were measured with an infrared PowerRefractor. Power of the vertical meridian was recorded for subjects viewing far and near targets in free space and through a Badal lens apparatus with and without reading spectacles. Additionally, refractive measurements were taken after subjects wore +2D reading spectacles for 30 min (post-adaptation). In free viewing and viewing through the Badal lens, subjects uniformly over-accommodated relative to the target while wearing reading spectacles (i.e., with the spectacles, they focused at a plane in front of the target). Subjects in the first post-adaptation test showed no significant difference in accommodation between viewing a near target with and without +2D spectacles after having read with them for 30 min, though they had without post-adaptation. Subjects in the second post-adaptation test were not significantly differently accommodated before and after reading when binocularly viewing a near target with +2D reading spectacles. The results imply that no adaptation of the subjects' accommodative postures while viewing visual targets occurred as a result of a 1/2 h near work task with the spectacles. The over-accommodation of subjects using reading spectacles while they are performing visual tasks shows the necessity of measurement if their true accommodative posture is to be determined.

Compensation of corneal horizontal/vertical astigmatism, lateral coma, and spherical aberration by internal optics of the eye.

Both the anterior surface of the cornea and the internal optics (the posterior cornea, crystalline lens) contribute to the aberration of a wavefront passing through the eye. Artal, Guirao, Berrio, and Williams (2001) reported that the wavefront aberrations produced by the internal optics offset, or compensate for, the aberrations produced by the cornea to reduce ocular wavefront aberrations. We have investigated the wavefront aberrations of the cornea, internal optics, and complete eye on both the population and individual level to determine which aberrations are compensated and probable paths leading to that compensation. The corneal and ocular aberrations of 30 young subjects at relaxed accommodation were measured with the Topcon Wavefront Analyzer, which simultaneously measures refraction, corneal topography (videokeratoscope), and wavefront aberrations (Hartmann-Shack sensor). We found strong evidence for compensation of horizontal/vertical (H/V) astigmatism (Zernike term Z5) lateral coma (Z8) and spherical aberration (Z12). H/V astigmatism compensation is scaled for each individual, suggesting that it is actively determined by a fine-tuning process. Spherical aberration shows no individual compensation, suggesting that is a passive result of genetically determined physiology. Lateral coma shows individually scaled compensation, some of which may be attributable to eccentricity of the fovea.

The allometry and scaling of the size of vertebrate eyes.

We compiled data from the literature and colleagues to examine the relationship between eye axial length and body weight for vertebrates as well as birds, mammals, reptiles, and fishes independently. After fitting the data to logarithmic and semi-logarithmic models, we found that axial length of vertebrate eyes does obey a conventional logarithmic relationship with body weight rather than a semi-logarithmic relationship as suggested by the results of previous studies. The regression slopes and intercepts appear to be characteristic of various animal groups. The axial length of the eye is largest in birds and primates, smaller in other mammals (especially rodents) and reptiles, and widely varying in fishes.

Measurement of refractive state and deprivation myopia in two strains of mice.

PURPOSE: The mouse eye has a bright retinal image (f/number <1) but low optical quality (visual acuity about 0.5 cpd) that may render emmetropization unnecessary. However, this species is potentially a powerful model to study eye growth and myopia because its genome can be readily manipulated and has been completely sequenced. We have investigated how precisely eyes of mice can be refracted and tested whether deprivation myopia can be induced by frosted diffusers. METHODS: An automated eccentric infrared photorefractor was adapted to refract eyes of two mouse strains--C57BL/6 (B6) and DBA/2 (D2)--during Tropicamide cycloplegia without anesthesia. Axial lengths were measured in highly magnified video images of freshly excised eyes. Plastic hemispherical diffusers were applied between postnatal days and 29 and left attached for 7 or 14 days. RESULTS: (1) Trial lenses ranging from +10 to -10 D produced high correlations between the brightness slope in the pupil and applied lens power (r = 0.81 and r = 0.87), demonstrating reliable refraction. Five repeated measures in 12 eyes showed an average standard deviation of 3.0 D, equivalent to an axial length change <10 microm (derived from schematic eye modeling). (2) Deprivation produced a significant shift toward myopia, relative to untreated eyes, but only after 14 days and only in B6 mice (p = 0.02 with or p = 0.00038 without one outlier; N = 9). In contrast, DBA/2J were unaffected by occlusion, perhaps due to mutations that target eye, lens, or anterior segment. (3) Both eyes of untreated animals often had axial lengths that differed markedly. Surprisingly, we detected no significant correlation between refractive error and axial length after treatment. CONCLUSIONS: The infrared refraction technique is sufficiently sensitive to resolve equivalent changes in axial length of only +/- 10 microm in alert mice. Prolonged occlusion produces a significant myopic shift in B6 mice, but not in D2 mice. Even among isogenic B6 mice, the response is variable for reasons that presumably trace back to subtle developmental, environmental, and technical factors.

The effects of constant and diurnal illumination of the pineal gland and the eyes on ocular growth in chicks.

PURPOSE: To investigate the effects of constant or 12-hour cyclic illumination of the pineal gland and the eyes on the growth of the chick eye. METHODS: Chicks (Gallus gallus, Cornell K Strain) were raised either under a 12-hour light-dark cycle of normal light or under constant light, with or without opaque removable hoods that covered the top of the head for 12 hours each day. A second group of chicks was raised under constant light with opaque eye covers that were worn on either both eyes or only the right eye for 12 hours each day. Chicks were placed in the experimental conditions on the third day after hatching and raised for 3 weeks. RESULTS: Pineal gland hoods and eye covers worn 12 hours a day significantly (P < 0.0001) protected the chicks from hyperopia under constant-light conditions. They also reduced the flattening of the cornea caused by constant light. Most striking was the protection afforded the uncovered eye from constant light's effects by the periodic covering of the opposite eye. CONCLUSIONS: A diurnal light-dark rhythm presented to one of three photosensitive organs (the pineal gland and both eyes) can protect the eyes from the effects of constant light. This is most probably due to the maintenance of a melatonin rhythm in the organ receiving the diurnal light rhythm.

Clinical features of the retinopathy, globe enlarged (rge) chick phenotype.

The purpose of the study reported here was to characterize the clinical aspects of the autosomal recessive retinopathy, globe enlarged (rge) phenotype in chicks (Gallus gallus). Rge/rge, rge/+ and +/+ chicks were studied from hatch to 336 days of age by general clinical examination, post-mortem examination, vision testing with an optokinetic device, ophthalmoscopy, biomicroscopy, tonometry, central corneal pachymetry, a-mode ultrasonography, infrared photoretinoscopy and photokeratometry. Additionally, preliminary electroretinographic and histopathologic investigations were performed. There is a variable degree of vision loss in rge/rge chicks at 1 day of age with further chicks losing vision over the next few weeks until all chicks become functionally blind by 30 days of age (although some optokinetic responses remain in some of the rge/rge chicks). Over the first few weeks of life rge/rge chicks develop thicker corneas with a larger radius, hyperopia, shallower anterior chambers and enlarged globes both radially and axially, compared to controls. A preliminary ERG study showed that 1 day old rge/rge chicks have an elevated response threshold, a lower amplitude a-wave with a markedly shallow leading slope, a lack of both oscillatory responses and c-waves and, at brighter flashes, an increased b-wave amplitude. Light microscopy revealed no gross retinal abnormalities in young chicks to account for the blindness. A thinning of all retinal layers developed in parallel with globe enlargement. The rge defect is a unique progressive retinal dystrophy that results in a severe visual deficit, abnormal electroretinographic waveforms, and secondary globe enlargement.

Corneal power and underwater accommodation in great cormorants (Phalacrocorax carbo sinensis).

In great cormorants (Phalacrocorax carbo sinensis), corneal refractive powers, determined by photokeratometry, ranged between 52.1 diopters (52.1 D) and 63.2 D. Photorefractive reflexes, determined by infrared video photorefraction, indicated that in voluntary dives the cormorants accommodate within 40-80 ms of submergence and with myopic focusing relative to the photorefractor attained when prey was approximately one bill length from the plane of the eye. Underwater, the pupils were not constricted and retained diameters similar to those in air. These results support previously reported capacities of lenticular changes in amphibious birds yet do not fully correspond with earlier reports in terms of the coupling of iris constriction with accommodation, and time course.

High order wave aberration of eyes.

This paper is concerned with the means and distribution of the wavefront variances and their root mean squares (RMS) of normal eyes, as measured by various techniques and computed for various pupil sizes. Using data from a subjective crossed cylinder aberroscope [Howland and Howland J. Opt. Soc. Am. A 67(1977)1508] it was found that the logarithms of the wavefront variances are approximately normally distributed. A comparison of data from this subjective study with that of six other studies using a variety of techniques of wavefront measurement showed that the relationship between RMS wavefront deviations of high order aberrations (third order polynomial terms and above) obeyed the relationship: log (RMS) (microm) = -1.918 +/- 0.048 SE + 3.023 +/- 0.111 x log (pupil radius) (mm), with R2 = 0.971.