Abstract
purpose. To induce form deprivation myopia in fish and investigate the role of the lens in the development of refractive error.
methods. Tilapia (Oreochromis niloticus), approximately 4 months old and from 26 to 63 g, were divided into three groups. Translucent goggles were directly sutured over the right eye for 4 weeks to induce form-deprivation myopia; the left eye served as an untreated contralateral control. The refractive state was measured by retinoscopy. Ocular dimensions were determined from frozen sections and with ultrasound biomicroscopy, and a scanning laser system was used to determine the optical quality of excised lenses.
results. After 4 weeks of form-deprivation treatment, all the deprived fish eyes showed development of significant amounts of myopia ranging from −3.75 to −26.25 D, with the average amounting to −10.27 ± 1.14 D. Eye dimension measurements show that the vitreous and anterior chambers of the treated eye are significantly longer axially than those of the contralateral eyes. No significant change in optical quality was found between lenses of the myopic and nonmyopic eyes. The fish recovered completely from the myopia 5 days after the goggle was removed.
conclusions. Although lower vertebrates are capable of lifelong growth, their eyes are susceptible to form-deprivation myopia. Thus, the visual environment is an important factor controlling ocular development in lower vertebrates, as well as in higher ones, and eye development is not strictly genetically determined. This study also indicates that lens growth and optical development are largely independent from the refractive development of the whole eye.
Reports published over the past 25 years have established that the refractive development of the eye can be altered by manipulating the visual environment during early development through the use of translucent goggles to deprive the eye of clear form vision
1 2 or by the use of defocusing lenses.
3 Form deprivation usually results in the induction of myopia.
4 Later work includes the use of convex and concave defocusing lenses to induce both myopia and hyperopia.
3 5 Form-deprivation myopia has been induced experimentally in a wide range of mammalian species including monkeys,
1 marmosets,
6 tree shrews,
7 cats,
8 guinea pigs,
9 squirrels,
10 and mice.
11 12 Form-deprivation myopia has also been demonstrated in human infants with neonatal eyelid closure and in birds such as chicks
2 and kestrels.
13 Chicks, which grow rapidly and exhibit a large repertoire of defocus lens-induced refractive errors, including myopia, hyperopia, and astigmatism,
5 are the most common animal model of refractive development. Even with the optic nerve sectioned, visual deprivation causes myopia in chicks,
14 suggesting that local retinal factors control eye growth.
Accommodation has been implicated as one factor leading to myopia in humans,
15 16 and the strong correlation between near work and development of myopia seems to support this idea,
17 18 but the evidence from animal experiments strongly suggests that accommodation is not essential to the control of eye growth. This point is also highlighted by a study reported by McBrien et al.
10 in which myopia was induced in gray squirrels (
Sciurus carolinensis), a diurnal mammal with little or no accommodative ability. That chicks are able to recover from induced refractive error, even when accommodation is eliminated by optic nerve section
14 or by lesions of the Edinger-Westphal nucleus,
19 also makes this point.
Although these and other studies have shown that there is a relationship between the visual environment and early eye growth and refractive development, the genetic factors involved are not clear. In humans, many studies have revealed a positive relationship between parental myopia and myopia in children,
20 and a light and focus-dependent relationship has been noted in relation to the expression of the transcription factor ZENK in the chick retina.
21
As noted, the work involving experimentally induced refractive error has been performed on higher vertebrates, essentially birds and/or mammals. More specifically, the experiments are performed on young, early postnatal, or posthatching animals, during the period of maximum eye growth and plasticity. In fact, if the cause of the induced error is removed early enough, be it a translucent goggle or a defocusing lens, the eye under treatment returns to a normal, emmetropic, refractive state. Experimental treatments performed during later stages of development yield smaller refractive changes and are less likely to show complete recovery when the goggle or lens is removed.
22
This report deals with the question of whether the eyes of lower vertebrates, such as fish, would respond to the same type of manipulation of the visual environment. We asked this question in the context of studying a group of vertebrates that are capable of growth and development throughout their lives.
23 Either the eye is susceptible to the visual environment throughout life, or eye growth and development is solely driven by genetics.
There have been few studies concerning the development of refractive error in lower vertebrates. Kröger and Wagner
24 reported, in a study of the effect of wavelength in the aquatic environment, that the eye of the blue acara (
Aequidens pulche, Cichlidae) grows to compensate for defocus due to chromatic aberration. Kröger et al.
25 found that dopamine depletion has no effect on the influence of the visual environment on eye growth. This research included a form-deprivation effect produced by using 2.5% glutaraldehyde in phosphate-buffered saline to make the fish cornea translucent. The treatment was applied every 3 days to keep the cornea translucent, but no significant change in axial length of the eye was noted.
Among vertebrates, fishes are the largest group (25,000 species).
26 Fish, including their eyes and retinas, can continuously grow over a lifetime.
27 The fish cornea is essentially nonrefractive because of the close similarity between the refractive index of water externally and aqueous humor internally.
28 Thus, the lens is the only significant refractive component of the fish eye. In most fish, the lens, which is spherical in shape, protrudes through an immobile pupil. Accommodation in fish involves moving the lens along the pupillary plane or pupillary axis,
29 30 a very different mechanism from that of birds and mammals, which accommodate mainly by deforming the lens. The research described here involves the use of tilapia (
Oreochromis niloticus), a hardy species capable of rapid growth in culture, as a model of fish eye development. Moreover, tilapia belong to the Cichlidae family, a group containing several visual species.
25 25 31 Myopia was induced in three groups of tilapia by covering one eye with a translucent goggle for 4 weeks, and the contralateral eye served as the control. Refractive state and anterior eye dimensions were measured in anesthetized fish with a retinoscope and ultrasound biomicroscopy, respectively. Intraocular dimensions of enucleated eyes were measured by freeze sectioning, and lens focal properties were determined in vitro with a scanning laser.
Tilapia (O. niloticus) weighing between 26 and 63 g were obtained from a local fish farm (Northern Tilapia Inc., Bondhead, Ontario, Canada), kept in aquariums with cycled and filtered water at 28°C and fed with tilapia fish food (3PT Regular; Martin Mills Inc., Elmira, Ontario, Canada). The size of fish used was chosen for ease of handling, as well as to take advantage of the accelerating phase of tilapia growth. The relative growth rate, which is expressed as a percentage of increased body weight, decreases from 50% every 3 days in fry to 1% per day in fish over 1 pound. To accelerate fish growth, the fish were fed three times each day. Fluorescent lighting in the aquarium room was set to a diurnal (12-hour light–dark) schedule. All fish were cared for according to the Guidelines of the Canadian Council on Animal Care and in accordance with the policies of the University of Waterloo and the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research.
Lightweight translucent plastic goggles were directly sutured over one eye, the treated eye, for 4 weeks. The right eye was always the treated eye and the left eye served as a contralateral control. Two or three sutures were sewn to the skin or soft bones around the orbit using nylon cosmetic stitches through holes in the edge of the plastic goggle. The fish did not appear to be disturbed by the goggle. In fact, a concurrent study of tilapia cortisol levels as an indication of stress from experimental handling did not indicate that the animals were experiencing difficulty (Shen W, unpublished data, 2004). Refractive state and fish weight and length were measured before and after the treatment. Anterior chamber depths were measured for both treated and untreated eyes at the end of the 4-week treatment period. At the end of the experiment, the fish were killed with an overdose of 2-phenoxythanol (3 mL/L) and the globes, both treated and untreated, were enucleated. Axial dimensions of both eyes were measured by freeze sectioning.
The experiments were performed on three groups of fish and were denoted as experiment 1 (n = 10), experiment 2 (n = 8), and experiment 3 (n = 9), after considerable preliminary experimentation with various types of translucent occluders, sutures, and suture techniques. An effort to produce visual deprivation by suturing the margins of the conjunctiva together was abandoned after it was found that this method resulted in pressure on and deformation of the cornea. The fish used in these experiments were weighed and measured at the start and end of each experiment. Eyes from experiment 1 were used in freeze-section measurements, whereas fish of experiment 2 were used for ultrasound biomicroscope measurements and for measurements of lens focal characteristics. In experiment 3, the goggles were removed after the induction of myopia, and the rate of recovery from myopia was determined.
Refractive state was measured with a streak retinoscope and trial lenses at a working distance of 25 cm through the glass wall of a specially designed narrow aquarium, whereas the fish were anesthetized with 0.6 mL/L 2-phenoxythanol to fix the direction of gaze and to minimize accommodation. The results were an overestimation of the refractive error in the hyperopic direction,
32 due to the difference in refractive index of water and glass, and the true refractive error was obtained by dividing by 1.33.
For freeze sectioning, both eyes were enucleated, immersed in a freeze-section medium (Stephens Scientific, Little Rock, AR), and then frozen immediately by being placed into dry ice. Marks made on the eyes with indelible ink when the fish were first killed identified the nasal and temporal limbi, the apex of the cornea and posterior scleral exit point of the optic nerve. The eyes were freeze sectioned on a cryostat microtome until a horizontal section through the geometric axis of the eye (premarked with indelible ink) was apparent. A loupe with a scale (± 0.1 mm) was placed on the section, and a photograph was taken with a digital camera. Later, the digital image of the hemisectioned eye was transferred to a computer and processed with ImageJ (available by ftp at zippy.nimh.nih.gov/ or at http://rsb.info.nih.gov/nih-image; developed by Wayne Rasband, National Institutes of Health, Bethesda, MD). The dimensions measured, included total axial length, anterior (cornea to lens) and posterior chamber depths, and lens diameter.
Cornea-to-lens distance was also measured with live anesthetized fish by using an ultrasound biomicroscope (UBM; model P40; Paradigm Medical Industries, Inc., Salt Lake City, UT). In this case, the fish was maintained in water in a fixed position so that the iris plane was perpendicular to the scanning plane of the probe. Six scans were obtained of each fish and the results averaged. The average anterior chamber depth was measured from the inner surface of the cornea to the lens surface and to the iris plane, respectively.
Measurements of lens focal characteristics were performed to detect whether there was a change in lens optical quality. After each fish was killed, both lenses were scanned with an automated laser scanning system developed at the University of Waterloo. A low-powered helium-neon laser beam passes up through a small window at the bottom of the scanner, at various motor-controlled x–y coordinates from the center. The directions of refracted beams are captured with digital cameras. Before scanning, the optical axis of the lens is determined by locating the position of minimum or zero beam deviation. Lenses were scanned at various eccentricities from the optical axis, and back vertex focal lengths (BVFLs) were recorded and stored in the computer. The data from the lenses of the treated and untreated eyes were compared, to determine whether visual form deprivation affects lens optical development.
Experiment 1.
Experiment 2.
Experiment 3.
Ultrasound Biomicroscope.
Freeze Sectioning.
This work shows that form-deprivation myopia can be induced in lower vertebrates, as in higher vertebrates, when the eye is deprived of clear vision. In fact, the 0.20-mm difference in vitreous chamber depths between form-deprived and untreated eyes
(Table 1)may be correlated with lens focal lengths of approximately 4.0 mm (average BVD plus lens radius;
Table 1 ,
Fig. 4 ). These values show dioptric differences for a lens in water of 8 to 9 D, or an amount close to the average myopia measured. This finding is strong evidence that all vertebrates share the same mechanism by which the visual environment controls eye growth. Because the cornea is essentially not a refractive structure under water and the focal properties of the lens are not altered, myopia results from an elongation of the vitreous chamber
(Table 1) .
In this study, the refractive states of tilapia were measured in the lateral direction—that is, in the direction perpendicular to the pupil plane, This direction is generally the one of least accommodation in fish,
29 31 and the refractive state of untreated tilapia eyes is similar to that of the common bluegill (
Lepomis macrochiris) when accommodation is diminished with atropine.
29 The average tilapia refractive state of from 1 to 3 D of hypermetropia agrees with the Glickstein and Millodot
33 curve relating eye size and apparent hypermetropia. After 4 weeks, all the goggled eyes in the experiments developed myopia (3.75–26.25 D), compared with either the measurements of the goggled eye before treatment or the contralateral control eye.
The result showing an increase in vitreous chamber depth is comparable to the findings of other animal experiments, the difference being that other experiments are performed only at an early growth stage, just after birth or hatching. The fish of this study were approximately 3 to 4 months old. They were selected for their size in relation to the experimental procedures, although it is known that tilapia are sexually mature at 5 to 6 months at any size.
34
In contrast to fish, there is a specific period of plasticity in higher vertebrates such as tree shrews, chicks, and primates, during which the eye is sensitive to visual manipulations.
35 Because fish can grow through life, it should be possible to manipulate eye growth at any age. However, because growth rates vary with age, we assume that the susceptibility of the eye to environmental influence varies. In addition, higher vertebrates demonstrate an emmetropization process from hypermetropia to emmetropia after birth or hatching.
36 37 In chicks, the hypermetropia decreases from +6 D after hatching to +2 D by 16 days,
38 and a human infant study suggests that emmetropization may be visually guided.
39 In the present study, the fish are hypermetropic. Although this question was not specifically addressed in our study, it appeared that larger fish were less hypermetropic. After 4 weeks of treatment, the untreated eyes also become slightly less hypermetropic or more myopic, the average before and after difference being 1.42 ± 0.36 D (paired
t-test,
n = 17,
P = 0.001) and this difference may simply reflect the emmetropization process.
From the results of experiment 3, it is noted that the induced myopia completely recovered within 5 days, along with decreased variability of refractive errors, as in a tree shrew study.
40 Recovery processes in both animals appears to be visually guided. Recovery was also found in other higher vertebrates, such as chick
22 and monkey,
41 in which change in choroid thickness is involved. The thickness of the choroid in fish species such as tilapia is substantial (∼0.3–0.4 mm in the fish used in this study) and therefore the role of the choroid, especially in recovery from myopia, merits future study, along with an examination of change in lens focal length and eye size.
30
As noted earlier, it was found that there is a significant correlation between induced myopia and difference of vitreous chamber depth measured from the iris plane to the retina. This is evidence that freeze sectioning is a dependable method for the measurement of fish eye dimensions. In contrast, no significant correlation was found between the amount of induced myopia and the change in fish weight or growth rate. Eye growth therefore appears to be independent and under local control in response to the altered visual environment.
Although with the freeze-sectioning method, we were able to demonstrate differences in eye size as a result of form deprivation, the approach is not sensitive enough to monitor accurately the eye growth taking place normally over the 4-week deprivation period. A more focused study involving the use of a breeding population of fish is needed to evaluate and quantify tilapia eye growth characteristics. For example, in the blue acara study, Kröger and Wagner
24 referred to earlier involved use of laboratory bred fish that were maintained in a variety of light conditions for a 6-month period. In the current tilapia study, the fish were purchased on the basis of weight without precise knowledge of age. However, freeze-sectioning measures of 15 untreated contralateral eyes show a strong correlation between fish weight and axial length of the eye, with weights ranging from 41 to 101 g and corresponding axial lengths ranging from 5.79 to 7.16 mm.
As also noted before, the induced myopia results in an increase of vitreous chamber length and cornea-to-lens distance. These changes are similar to the appearance of the eye of black moor gold fish, a genetic example of extreme myopia.
42 Although study of higher vertebrates has led to variable conclusions regarding change in cornea-to-lens distance,
2 20 36 43 44 in fish, whatever the cause, myopia appears to be accompanied by an increase in anterior chamber depth.
The results of this study, both in terms of focal length measurements and from freeze-section analysis, are also consistent with earlier work with higher vertebrates, in that the lens of the eye is not obviously affected by form deprivation. McKanna and Casagrande
45 reported that lens thickness is diminished with form deprivation in tree shrews. Priolo et al.
46 noted that although lens focal length was unaffected, lens spherical aberration (nonmonotonic focal variability) increases when hyperopia and high levels of myopia are induced in chicks. However, because focal length is not changed, the lens does not contribute directly to the change in refractive state.
In addition to the lens, retinas of adult teleost fish continue to develop,
27 and eye size increases with growth throughout life. Thus, the fish eye remains in a lifelong plastic state, and its refractive development is continuously susceptible to the influence of the visual environment.
Supported by a grant from the Natural Sciences and Engineering Research Council of Canada (JGS).
Submitted for publication November 10, 2004; revised December 21, 2004; accepted January 14, 2005.
Disclosure:
W. Shen, None;
M. Vijayan, None;
J.G. Sivak, None
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked “
advertisement” in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Corresponding author: Jacob G. Sivak, School of Optometry, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada;
[email protected].
Table 1. Average Intraocular Dimensions for Untreated and Treated Tilapia Eyes after 4 Weeks of Unilateral Form Deprivation
Table 1. Average Intraocular Dimensions for Untreated and Treated Tilapia Eyes after 4 Weeks of Unilateral Form Deprivation
| Eye Dimension | OD (mm) Form-Deprived) | OS (mm) (Untreated) | P (Paired t-test) |
| Nasotemporal diameter | 8.04 ± 0.12 | 7.99 ± 0.11 | 0.15* |
| Cornea–retina | 6.56 ± 0.08 | 6.19 ± 0.08 | <0.0007 |
| Anterior lens–retina | 5.94 ± 0.09 | 5.74 ± 0.08 | <0.005 (0.002) |
| Anterior chamber (iris plane–cornea) | 0.48 ± 0.04 | 0.31 ± 0.04 | <0.05 (0.01) |
| Lens diameter | 3.03 ± 0.07 | 3.07 ± 0.07 | 0.38* |
| Vitreous chamber 1 (iris–retina) | 4.80 ± 0.09 | 4.60 ± 0.07 | <0.005 (0.003) |
| Vitreous chamber 2 (posterior lens–retina) | 2.81 ± 0.05 | 2.60 ± 0.04 | <0.005 (0.004) |
The authors thank Nancy Gibson, Robin Jones, Kelley Moran, and Vladimir Bantseev, for assistance during the study.
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