Free
Lecture  |   March 2004
Through the Lens Clearly: Phylogeny and Development
Author Affiliations
  • Jacob G. Sivak
    From the School of Optometry, University of Waterloo, Waterloo, Ontario, Canada.
Investigative Ophthalmology & Visual Science March 2004, Vol.45, 740-747. doi:10.1167/iovs.03-0466
  • Views
  • PDF
  • Share
  • Tools
    • Alerts
      ×
      This feature is available to authenticated users only.
      Sign In or Create an Account ×
    • Get Citation

      Jacob G. Sivak; Through the Lens Clearly: Phylogeny and Development . Invest. Ophthalmol. Vis. Sci. 2004;45(3):740-747. doi: 10.1167/iovs.03-0466.

      Download citation file:


      © ARVO (1962-2015); The Authors (2016-present)

      ×
  • Supplements
The adaptive radiation of the eye from an optical perspective has long intrigued scientists, at least from the 19th century. In a paper on the optics of the fish lens published in 1816, David Brewster, the Scottish scientist, wrote, “There is, perhaps, no subject in natural history which has excited so much attention, as the structure and functions of the eyes of animals; … and the natural philosopher, considering it as the work of infinite intelligence, ardently anticipated the improvement of optical instruments from the imitation of this perfect model.” Thus, Brewster refers to the fundamental interest in the natural history of the eye as well as the potential benefits, or applications, this interest can lead to. A little later, in the 20th century, August Krogh, 2 the Danish physiologist and Nobel laureate, wrote in regard to the value of comparative animal research in general that “for almost every physiological problem there is an animal on which it can be best studied.” Two examples that come to mind include the use of the giant squid axon by Hodgkin and Huxley 3 to clarify the mechanism of neuronal impulse conduction and the study of the neural response of the compound eye of Limulus (the horseshoe crab), to examine the process of lateral inhibition. 4 Additional examples will be highlighted in the review that follows. 
The optical characteristics of the eye have been and continue to be a focus of comparative interest, and nobody has done more to draw attention to the optical solutions that have evolved among vertebrates than Gordon Walls in his opus titled The Vertebrate Eye and its Adaptive Radiation. 5 The fascination with the study of the varied optical elements of the eye, generally the structure and function of the cornea and lens and the mechanism of accommodation, stems in large measure from interest in how living biological tissue can operate in a physical sense to produce retinal images of good quality. 
Convergent Evolution: Fish and Cephalopod Lenses
Convergent evolution—that is, the independent development in different species of similar optical characteristics to deal with similar environmental pressures—is a prominent theme in Walls’ book, 5 and in other comparative reviews of the vertebrate eye. 6 In fact, it is commonly accepted that the eye evolved more than once. For example, Wald, 7 in a review dealing with the distribution and evolution of visual systems and based on the distribution of visual pigments, believed in three separate developments: the simple eyes of vertebrates and mollusks and the compound eye found among arthropods. More recently, this view has been challenged by Gehring, 8 who believes in a monophyletic origin of the eye on the basis of the common use of rhodopsin in metazoan eyes as a photoreceptor molecule and on the discovery of a universal master control gene, Pax 6, for eye development. The review that follows does not address this issue directly, although the similarities of optical solutions to common optical problems are probed to a fairly subtle level. Whether eye development is monophyletic or polyphyletic does not alter the fascination provided by the discovery of the existence of common solutions to common optical problems. One obvious example is the tapetum lucidum, a reflective layer of the choroid, or the pigmented epithelium of the retina, which is found in many nocturnal species and is designed to enhance the probability that light energy will be absorbed by the retinal photoreceptors. Although the morphology and chemical nature of the reflective material of this adaptation may vary among species, tapeta are found in virtually every major vertebrate group. 5 However, it is the similarities between cephalopod and vertebrate eyes that have been cited as particularly obvious examples of convergent evolution. 9 10 Not the least of such similarities is the existence of a spherical or nearly spherical lens responsible for focusing light on the retina. 
All vertebrate lenses are cellular ectodermal structures that develop initially as surface invaginations in sequence with the developing optic cup. 11 The early embryonic lens, consisting of a single layer of epithelial cells, forms a spherical hollow vesicle that is filled by the elongation of the posterior cells. Continued development of the lens through life takes place through mitotic activity and growth around the lens equator, with new cells, the secondary lens fibers, forming shells around the posterior outer lens surface and under the anterior layer of epithelial cells. This continued development, with older tissue located centrally, results in the formation of a lens with a gradient refractive index in which the index increases from the lens periphery to the core. 
In aquatic vertebrates, such as fish, the lens is the only significant refractive element of the eye. 12 The teleost lens is usually portrayed as spherical in shape and having a constant relative focal length, known as Matthiessen’s ratio, of 2.55 (lens radius to focal length). 5 Although in some fish, notably elasmobranches, the lens is not spherical and the ratio of lens radius to focal length is not always a constant, 12 the spherical shape predominates. Not only does the lens represent the optical quality of the whole eye, but because the fish pupil is usually immobile, the eye operates at low F-stop levels at all times, and the iris cannot shield the retina from aberrant light rays. Indeed, in many species, pupil diameter exceeds lens diameter. The fish lens is particularly interesting with respect to spherical aberration, because whatever aberration exists cannot be neutralized by corneal aberration of opposite sign. Because the lens is spherical, lens shape is not a factor in the control of spherical aberration and the variation of lens refractive index resulting from continual lens development is the only means by which the aberration is minimized (Figs. 1 2) . The use of the fish lens to examine the relationship between lens optical quality and its gradient refractive index is another example of the principle articulated by Krogh. 2 Also, because fish accommodate by lens movement (see the next section below), rather than by a change in lens shape, spherical aberration is not affected. 
The cephalopod (e.g., squid, octopus) lens develops as two roughly hemispheric halves from two separate ectodermal (lentogenic) sources. 13 14 The posterior lens primordium appears first during development, to be followed later by the anterior lens primordium, which initially forms a cap over the former. Both segments are derived from cell processes that fuse during morphogenesis to form concentric shells or plates. As in the case of the vertebrate lens, the cephalopod lens is composed of soluble proteins (in squid these are the S-crystallins), which form first in the posterior lens segment and lentogenic body. 15 Moreover, as with the vertebrate lens, the cephalopod lens continues to grow and form crystallins during adulthood. The two lens components, which meet at a central interface, the septum, are not equal in size. The posterior segment is larger, forming 55% to 60% of the axial lens diameter. 16 17 Whereas spherical aberration is largely neutralized, as in vertebrates, through a gradient variation in refractive index, the cephalopod lens does not exhibit the optical quality of the teleost lens. This difference may not be a problem as far as vision is concerned. Unlike the teleost, in which pupil mobility is rare, the ability of the cephalopod pupil to respond in size to varying levels of illumination can shield the retina from contributions to the retinal image by the lens periphery, at least in diurnal conditions. Thus, although the two lens types are similar in shape and in the existence of a gradient refractive index, they are very distinct embryologically and in optical quality, as well as in the indication that the cephalopod lens is a cell product. 
This comparison of the lenses of the eyes of fish and cephalopods does not address the question of whether the eye has a single phyletic origin or whether it evolved more than once. Nevertheless, it is a useful point to keep in mind as more detailed experimental knowledge of the field of comparative visual optics becomes available. 
Accommodation in Teleosts
In teleosts, or modern boney fish, it has been known for more than a century that the lens is not deformed during accommodation, but is moved within the eye by a smooth muscle, the retractor lentis. The muscle, first described in 1834 by Wallace, 18 originates at the anterior end of the falciform process, a vascular structure located in the embryonic fissure of the optic cup, which in most species remains open. 5 19 In 1894 Beer 20 noted that when the excised fish eye was stimulated electrically the retractor lentis contracted and moved the lens toward the retina. Similar results were obtained by Somiya and Tamura 21 and by Somiya. 22 That the retractor lentis is innervated by postganglionic parasympathetic nerve fibers was established by Meader 23 on the basis of a study of stained serial sections from the teleost genus Holocentrus. Thus, I 24 was able to use a parasympathomimetic and a parasympatholytic to induce accommodative contraction and relaxation of the retractor lentis muscle in several freshwater teleosts to show that the magnitude and direction of lens movement correlates with the feeding behavior of each species. Somiya 22 confirmed that the retractor lentis is parasympathetically innervated by the oculomotor nerve through the radix brevis in bass and mackerel. Electrical stimulation of the short ciliary nerve, which contains both parasympathetic and sympathetic fibers, causes contraction of the retractor lentis, whereas stimulation of the sympathetic ganglion does not. 
Meader 23 demonstrated that the retractor lentis is composed of smooth muscle fibers, and Munk 25 observed two separate components, a lateral muscle and a medial muscle in teleosts from the families Blenniidae and Clinidae. In the oscar (Astronotus ocellatus), a cichlid indigenous to northern South America and Florida, 26 the retractor lentis is a single pigmented triangular muscle originating from the pars retinas terminalis and inserting by a transparent ligament on to the ventral surface of the lens. 19 In a specimen measuring 10 cm overall, the lens measured 5.2 mm in diameter, whereas the base and height of the muscle measured 2.8 and 3.8 mm, respectively. There is an additional iris insertion, possibly a stabilizing feature, from the midpoint of the muscle to just below the inferior edge of the pupil. The muscle is innervated by the short ciliary nerve, which pierces the sclera along with the optic nerve. The main branch of the nerve terminates on the posterior surface of the muscle. Stimulation of the nerve results in accommodative lens movement but no pupillary constriction. Two distinct muscle fiber orientations are seen in light micrographs of the retractor lentis. 
Most of the literature on accommodation in teleosts involves the use of artificial stimulants and nonliving or drugged fish and /or excised eyes. However, Sivak and Howland 27 used a video recording system to measure the magnitude and speed of the natural accommodative response of the rock bass (Ambloplites rupestris) to a feeding stimulus. A similar approach was taken to measure accommodation in the oscar (Astronotus ocellatus) as a function of feeding stimuli located at varying distances from the fish. 28 Food targets were introduced at 48, 20, 12, and 4 cm from the oscars while eye and lens position were recorded and later analyzed frame by frame. The results indicate that the lens is capable of both nasal–temporal and medial–lateral movement, a finding that agrees with the dual orientation of the retractor lentis muscle fibers. These two components occur independently or together. The greatest relaxation of the muscle occurs with the nearest target (4 cm), producing sample lens movements of 0.33 mm nasal-temporally and 0.12 mm medial-laterally. The largest lens movements take place along an axis 22° from the pupillary plane. This axis, the visual axis, probably corresponds to the retinal location of maximum photoreceptor density. 29 30  
In humans, differences between the accommodative stimulus and the accommodative response are referred to as the lag and lead of accommodation, with lag (insufficient accommodation, or hyperopia) prevalent at the nearest target distances and lead (excess accommodation, or myopia) found for the farthest targets. 31 32 These differences, or errors, are necessary for the operation of a biofeedback control system in which accommodation acts as a proportional controller. 31 In other words, some defocus information is needed by the autonomic nervous system to guide the neuromuscular system responsible for providing the correct accommodative response. In spite of considerable morphologic and physiological difference between the teleost and human mechanisms of accommodation, and the fact that accommodative muscle contraction takes place for distant targets in the former and for near targets in the latter, the oscars demonstrate a lag of accommodation for the closest targets and an accommodative lead for the farthest ones (Fig. 3) , as has been noted in humans. 31  
The Avian Lens and Accommodation
Accommodative Apparatus: Ciliary Muscle
The avian accommodative mechanism differs markedly from that of mammals in that the force of contraction of the ciliary muscle is transmitted directly to the lens, rather than indirectly through the zonular (or suspensory) ligaments. 33 34 This direct articulation between the ciliary body and the lens is brought about by an exaggeration of the equatorial diameter of the lens due to the elongation of the equatorial epithelial cells to form the annular pad, or ringwulst; the existence of a pronounced cornea-scleral sulcus, maintained by a ring of overlapping limbal bones, the scleral ossicles; and the prominent and numerous ciliary folds, which extend a significant distance from the pars plicata of the ciliary body to the lens. Moreover, the avian ciliary muscle (as well as the sphincter and dilator muscles of the iris) are striated, showing ultrastructural characteristics consistent with fast muscle fibers, including clearly defined z-lines, abundant mitochondria, an extensive endoplasmic reticulum, and the common appearance of transverse tubules at A-I junctions. 35 This is true despite the fact that the muscle is innervated by the postganglionic parasympathetic fibers of the oculomotor nerve. 36  
This well-developed accommodative apparatus, coupled with the soft consistency of the avian lens, has produced an adaptation in certain aquatic species that makes it possible for the lens to compensate for the refractive loss of the cornea when the bird dives into water. 37 38 Thus, in birds such as the hooded merganser (Mergus cucullatus) and the common goldeneye (Bucephala clangula), two species that actively pursue their prey underwater, the eye is capable of rapid and large accommodative lens change (70–80 D) by means of a dramatic change in lens shape that results in the formation of an anterior lenticonus. The sphincter muscle of the iris plays a role in the change in anterior lens shape, although it is unclear whether this is produced actively or passively (by forcing the lens through a rigid annular opening) in these species. In this context, it has been noted that the iris sphincter is a more massive muscle in species that are pursuit divers, such as the hooded merganser. 35  
It has been shown that a number of birds, including the domestic chicken, accommodate by altering the curvature of the cornea, as well as by changing the shape of the lens. Corneal accommodation is accomplished through contraction of an anterior segment of the ciliary muscle, sometimes referred to as Crampton’s muscle. 39 In fact, the anatomy of the avian ciliary muscle varies and is confusing when it comes to the description of muscle groups. In birds, a ciliary cleft separates the ciliary body into an outer leaf composed of ciliary muscle, trabecular meshwork, and aqueous sinus and an inner leaf consisting of the fibrous base plate. 40 A detailed examination of the muscle in four species with differing natural histories (chicken, kestrel, pigeon, and hooded merganser), in the relaxed and the contracted states, shows that the muscle can be divided into three main muscle fiber groups on the basis of origin and insertion. 41 The anterior muscle fiber group originates at the sclera under the scleral ossicles and inserts into the inner lamellae of the cornea. During accommodation, these fibers pull the cornea posteriorly, reducing its radius of curvature and increasing its refractive power. The posterior muscle fiber group originates on the sclera and inserts posteriorly on to the base plate of the ciliary body. During contraction, the fibers pull the base plate forward and push the ciliary folds against the lens to alter its curvature. The third group of fibers, the internal group, extends from the base plate to the inner lamellae of the cornea and thus has a role in both corneal and lenticular accommodation. In general, most of the ciliary muscle fibers of the chicken, kestrel, and pigeon are in the anterior muscle fiber group, suggesting an emphasis on corneal accommodation. The ciliary muscle of the hooded merganser is largely made up of fibers in the internal and posterior muscle fiber groups, indicating, as expected from the need for acute vision in water, that lenticular accommodation predominates. 
Avian Lens
The development of the avian lens follows the usual vertebrate pattern, involving the formation and then filling of the lens vesicle and the continued development of new fibers (the secondary fibers) from the equatorial (germinative zone) epithelial cells. However, the secondary lens fibers taper sufficiently to meet at the two lens poles to form what are known as point sutures. This is in contrast to the line, or Y, or star sutures common to mammalian lenses, including those of primates. In the case of line or Y sutures, the overlapping of lens fibers in each successive shell is coincident and results in the formation of four or six three-dimensional suture planes that extend from the lens nucleus to the periphery. Optical analyses of excised rabbit (line sutures) and bovine (Y sutures) lenses, using a scanning laser system in which the refracted and then digitized beams are directed at various angles along and across lens sutures, have shown that the sutures can disrupt the optical quality of the lenses. 42 43 Moreover, the analysis of the bovine lens as a function of age indicates a deterioration, both optically and morphologically. 43 Morphologic changes include the development of more complex and irregular sutures and the development of an age-related compromise in the surface structure of individual lens fibers. In adult primates, the suture arrangement is more complex than that of rabbits and cows. Here it was determined that the existence of an offset arrangement of successive shells of lens fibers results in an optically superior lens. 44  
Study of the chicken lens both optically and morphologically as a function of age indicates that the advantage of the point suture is temporary, because with age the point suture spreads in width and is no longer in fact a point (Fig. 4) . 45 In addition, a deterioration in individual lens fiber surface anatomy occurs. 
Avian Accommodation and Age
A few relatively recent studies have examined chicken accommodation as a function of age. These include whole field electrical stimulation of the eye, 38 electrical stimulation of the Edinger-Westphal nucleus, 46 and the use of pharmacologic agents to stimulate accommodation. 39 More recently, Choh et al. 47 reported the results of a study in which accommodation was stimulated in excised chicken eyes of various ages by stimulating the ciliary nerve and ganglion by means of a suction electrode (Fig. 5) . The relationship between the ciliary body and lens remained intact, whereas immersion of the eye in water neutralized corneal refraction. The accommodative effect on lens focal length was measured directly through the use of a scanning laser system, as described earlier. In this preparation, the scanning beam enters the eye through the cornea and exits from a posterior opening so that its refracted orientation is visible to a television camera. 
All these studies indicate a loss of lenticular chicken accommodation with age. In the most recent model involving stimulation of the ciliary ganglion 47 chicken lenticular accommodation decreases progressively from an average of 22 to 23 D at hatching to a minimum level of approximately 2 D at 1 and 2 years (Fig. 4) . The decrease is precipitous initially, with accommodation approaching 10 D at 7 and 14 days and declining further to a little over 5 D by 6 weeks. 
The loss of accommodation with age, presbyopia, is of long-standing interest, and a considerable effort has gone into the study of its causes. Attention has focused on age-related changes in the human ciliary muscle as well as the age-rated loss of lenticular pliability. 48 In addition, change with age of the internal geometry of the eye, particularly the location of the suspensory ligaments relative to the location of the ciliary body and the lens, has been implicated. 49 The cause of presbyopia is probably multifactorial. 50 However, in the context of the avian eye, and mindful of the large and striated nature of the avian ciliary muscle, as well as the soft consistency of the avian lens, it may be reasonable to assume that age-related changes in internal eye geometry may be most important. 
Ametropia and Accommodation
During the past 25 years, the avian eye, particularly the chicken eye, has become common animal models of ocular refractive development. This is a result of the discovery that it is possible to induce myopia in species such as chickens and macaque monkeys by depriving the eye of clear form vision during early development. 51 52 In fact, earlier work such as that of Lauber et al., 53 demonstrated the plasticity of eye size in young chickens as a function of early visual deprivation. As a precocial bird that undergoes a rapid phase of early eye growth, the chicken has become the predominant species used in this research, because the manipulation of the visual environment can commence at hatching and the effects on eye development take place within days or hours. The chick is thus another clear example of an animal model in which a physiological problem can best be studied. 2 In 1988 Schaeffel et al. 54 demonstrated that it is possible to induce either myopia or hyperopia by using concave or convex lenses to defocus the retinal image, and Irving et al., 55 56 57 and others, have demonstrated the wide range of refractive states that can be induced using lightweight goggles and lenses. 
Although attention has focused on axial length change in studies of visually induced refractive error, the roles of the cornea and lens are less clear. Reports on corneal effects vary widely; with evidence indicating steepening, flattening, or no change, even in studies by the same investigators. The evidence is equally unclear as far as the lens is concerned. For example, two reports on the same species, cats, conclude that the lens is altered optically or not at all when refractive errors are induced. 58 59 Troilo et al. 60 noted that chick lens dimensions do not change in the case of deprivation myopia. In fact, a detailed examination of excised chick lens optical function, both before and after hatching, showed little or no change in focal length, even though the lens undergoes substantial change in size and shape, 61 possibly because changes in lens shape are neutralized by changes in refractive index distribution. The study was performed with a scanning laser system, as described earlier. Essentially, a helium-neon laser beam was scanned across the lens while equivalent focal length was measured for each beam position with a television camera. The lens axis was defined as the position showing no or minimum beam deviation. The absence of focal length differences, both paraxially and eccentrically, suggest that the developing chick lens is a static refractive component of the eye. That is, lens development is not influenced by the environment, but is strictly genetically programmed. 
on an earlier study with the same scanning laser approach, the investigators concluded that form deprivation myopia does not affect lens focal length, transmittance, or total lens soluble protein. 62 However, more recently, it has been noted that lenses from chick eyes in which myopia and hyperopia are induced show more spherical aberration than lenses from control eyes 63 although their focal lengths are more or less the same. The same lenses show no difference in weight, dimensions, or morphology. Thus, while the lens does not appear to contribute directly to the refractive error of the eye, lens optical quality is compromised, and it may be incorrect to conclude that the lens is influenced only by genetics. An effort to get at this question by examining lens crystallins from chick lenses of eyes in which myopia and hyperopia had been induced indicated no difference in αA- or δ-crystallin content in comparison with lenses from contralateral control eyes, 64 although the results suggest that the myopic and hyperopic treatments have different effects on δ-crystallin concentration. 
The possible connection between accommodation and the development of human refractive error, particularly myopia, has intrigued clinicians and scientists for well over 100 years. Nineteenth century scientists such as Donders 65 and von Helmholz 66 believed in an association between near work and development of myopia in children. Despite over a century of efforts to resolve this question, it remains an unresolved and controversial topic. In large measure, the recent growth of research into animal models of refractive error development has stimulated renewed interest into research related to human refractive development. The well-developed accommodative mechanism of the avian eye, coupled with the relative ease with which refractive errors can be induced in chicks, has led to several accommodation-related studies. In fact, as early as 1987, work with the chick model by Troilo et al. 60 showed that the phenomenon of form-deprivation myopia takes place even if the optic nerve is severed, thereby ruling out a controlling role for accommodation. However, further research indicates that the growth and refractive development of the eye is at least partially altered by the absence of afferent information from the optic nerve, 67 and thus it may be premature to rule out an accommodative role. Nevertheless, the role of accommodation does not appear to be significant, particularly with respect to providing information as to sign of defocus in the instances where concave and convex defocusing lenses are used. 
Recently, Choh 68 has used the chick model to examine whether experimentally induced ametropias will have an effect on accommodation (lenticular accommodation) and/or spherical aberration of the lens. In this work, myopia and hyperopia were induced in hatchling chicks through the use of translucent goggles (form deprivation) and 15-D convex lenses, respectively. After 7 days, the birds were killed, the eyes were enucleated, and the lenses optically scanned, using the in situ accommodation model described earlier, in which corneal refraction is essentially neutralized and the ciliary nerve/ciliary ganglion is stimulated. Lens focal properties were determined before during, and after accommodation. The results showed that focal lengths were significantly shorter in lenses from myopic eyes in comparison to their contralateral control eyes, whereas the focal lengths of lenses from hyperopic eyes were longer than those of lenses from control eyes. The amount of accommodation resulting from stimulation of the ciliary nerve and or ciliary ganglion was reduced in eyes in which myopia was induced in comparison to nonmyopic eyes, and greater in eyes in which hyperopia had been induced. However, although the amount of lenticular spherical aberration (always negative or overcorrected in the case of avian lenses) 63 increased with accommodation, there was no difference with respect to refractive state. 
Ultrasound biomicroscopy was also used to investigate accommodative changes of the anterior segment of the eye in relation to induced ametropia 69 and the results support the earlier study in demonstrating an ametropia-related effect on the accommodative apparatus. The preparation was similar to the in situ accommodation model described earlier and involved stimulation of the ciliary nerve to produce the accommodative effect. The primary difference in the two experiments is that, in this case, because the focal properties of the lens were not under investigation, the eye was left intact. As expected, accommodation always results in a decrease in anterior chamber depth, an increase in lens thickness, and steepening of the anterior surface of the lens, regardless of whether the eye was emmetropic, myopic, or hyperopic. However, the results also showed that in myopic eyes the anterior chambers were deeper and the lenses thicker than those from the contralateral control eyes. In the case of induced hyperopia, the anterior chambers tended to be shallower and the lenses thinner. 
The results of the two reports dealing with ametropia and lens optics 65 68 appear to be contradictory in that the first indicates no ametropia-related effect on lens refractive power, whereas the second does. The difference is very likely due to the lens’ isolation from its related structures in the first instance, whereas it remains connected to them in the second. Similarly, the effect of ametropia on accommodation is made evident by the in situ experimental approach used. As in the case of loss of accommodation with age, the effect of ametropia on accommodation may simply be due to differences in eye size and internal geometry. 
Summary
In the context of providing a review of selected issues in the field of comparative physiological optics, the first and introductory topic addressed deals with similarities and differences between the lenses of the eyes of fish and cephalopods. Although the two are similar in shape and gradient refractive index distribution, the optical quality of the cephalopod lens does not match that of its vertebrate counterpart, probably because the cephalopod lens is composed of two separate embryological components. This is in contrast to the development of the fish (vertebrate) lens from a single germinal source. The review continues with an examination of three additional comparative topics related to the study of lens development and accommodation. The first involves the study of accommodative lens movements in fish, a mechanism that is especially well developed in visual species such as Astronotus ocellatus, a cichlid. Typically, the dorsally suspended spherical lens is moved toward the retina, in response to a distant target, by contraction of the retractor lentis muscle. Despite the obvious differences between this mechanism and that of the human eye, a stimulus–response analysis indicates the same pattern of errors with respect to lag (insufficient accommodation) and lead (excess accommodation). 
Research into the effect of age and ametropia on accommodation in birds (chickens) is described next. The avian lens and the avian accommodative mechanism also differ significantly from that of the human eye. Essentially, the lens articulates with the ciliary processes so that the effect of ciliary muscle contraction is transferred directly to it. Moreover, the secondary fibers of the avian lens meet at the lens poles, or point sutures, rather than in the form of line sutures. Even with these differences, as well as the striated nature of the ciliary muscle, lenticular accommodative amplitude diminishes very significantly with age in chickens and the optical quality of the lens deteriorates as well. Part of this deterioration is caused by the gradual expansion and spreading of the anterior and posterior point sutures. Finally, when ametropia is induced by altering the normal retinal stimulus pattern of hatchling chicks, lens focal characteristics and the accommodative response are altered. In the case of induced myopia, lens focal lengths are shorter and accommodation is reduced, whereas the opposite is found with induced hyperopia. 
It is tempting to make comparisons between results obtained using animal models with data from human experiments, and, in keeping with the principle articulated by August Krogh, 2 to use the models of induced ametropia to explain the development of human refractive error. It is equally important to avoid overgeneralizing from such models. There are more than 50,000 vertebrate species (50% are fish) 70 with wide variations in life histories and visual need. Study of one species of a larger group, perhaps on the basis of availability or cost, or some other measure of convenience, may not reflect the visual status of the group as a whole. For example, a form-deprivation study of a nonprecocial bird, the American kestrel (Falco sparverius), produced results that differed substantially from typical chick form-deprivation data. 71 Thus, the use of animal models should not result in neglect of the need to continue widening the study of the comparative nature of the eye. 
 
Figure 1.
 
Photograph of a 6.0-mm diameter glass sphere in water refracting parallel helium-neon laser beams of two separations. The difference in focal lengths of the two separations showing positive (or undercorrected) spherical aberration, reflects the homogeneous refractive index of the sphere.
Figure 1.
 
Photograph of a 6.0-mm diameter glass sphere in water refracting parallel helium-neon laser beams of two separations. The difference in focal lengths of the two separations showing positive (or undercorrected) spherical aberration, reflects the homogeneous refractive index of the sphere.
Figure 2.
 
Photograph of a 6.0-mm diameter fish lens (rock bass, Ambloplites rupestris) in physiological solution refracting parallel helium-neon laser beams of two separations. The lack of a difference in focal length of the two separations is indicative of the absence of spherical aberration due to the developmentally related gradient refractive index.
Figure 2.
 
Photograph of a 6.0-mm diameter fish lens (rock bass, Ambloplites rupestris) in physiological solution refracting parallel helium-neon laser beams of two separations. The lack of a difference in focal length of the two separations is indicative of the absence of spherical aberration due to the developmentally related gradient refractive index.
Figure 3.
 
Accommodative stimulus-response functions for humans (left) (adapted, with permission, from Toates FM. Accommodation function of the human eye. Physiol Rev. 1972;52:828–863. © American Physiological Society. First appeared in Meas Control. 1972;5:58–61. © IEEE) and (right) a fish, the oscar (Astronotus ocellatus) (adapted, with permission, from Andison ME, Sivak JG. The naturally-occurring accommodative response of the oscar, Astronotus ocellatus, to visual stimuli. Vision Res. 1996;36:3021–3027. © Elsevier), showing similar accommodative lag and lead. Left and right: x-axis: stimulus (in diopters); y-axis: response (in diopters).
Figure 3.
 
Accommodative stimulus-response functions for humans (left) (adapted, with permission, from Toates FM. Accommodation function of the human eye. Physiol Rev. 1972;52:828–863. © American Physiological Society. First appeared in Meas Control. 1972;5:58–61. © IEEE) and (right) a fish, the oscar (Astronotus ocellatus) (adapted, with permission, from Andison ME, Sivak JG. The naturally-occurring accommodative response of the oscar, Astronotus ocellatus, to visual stimuli. Vision Res. 1996;36:3021–3027. © Elsevier), showing similar accommodative lag and lead. Left and right: x-axis: stimulus (in diopters); y-axis: response (in diopters).
Figure 4.
 
Scanning electron micrographs of the anterior sutures of 7-day, 2-year-old and 5-year-old chicken lenses (main lens body without annular pad) showing age-related spread in the “point” suture. The white bar (bottom right) represents 100 μm while the black lines outline the extent of the suture area (reprinted, with permission, from Priolo S, Sivak JG, Kuszak JR. Effect of age on the morphology and optical quality of the avian crystalline lens. Exp Eye Res. 1999;69:629–640. © Academic Press.).
Figure 4.
 
Scanning electron micrographs of the anterior sutures of 7-day, 2-year-old and 5-year-old chicken lenses (main lens body without annular pad) showing age-related spread in the “point” suture. The white bar (bottom right) represents 100 μm while the black lines outline the extent of the suture area (reprinted, with permission, from Priolo S, Sivak JG, Kuszak JR. Effect of age on the morphology and optical quality of the avian crystalline lens. Exp Eye Res. 1999;69:629–640. © Academic Press.).
Figure 5.
 
Loss of lenticular amplitude of accommodation with age in chickens as measured using an in situ physiological model in which the ciliary nerve is stimulated (reprinted, with permission, from Choh V, Meriney SD, Sivak JG. A physiological model to measure effects of age on lenticular accommodation and spherical aberration in chickens. Invest Ophthalmol Vis Sci. 2002;43:92–98. © Cadmus Professional Communications).
Figure 5.
 
Loss of lenticular amplitude of accommodation with age in chickens as measured using an in situ physiological model in which the ciliary nerve is stimulated (reprinted, with permission, from Choh V, Meriney SD, Sivak JG. A physiological model to measure effects of age on lenticular accommodation and spherical aberration in chickens. Invest Ophthalmol Vis Sci. 2002;43:92–98. © Cadmus Professional Communications).
The research involving the author’s laboratory, which is described in this review, included collaboration with a wide number of graduate students and colleagues over many years. Papers referenced were coauthored with Margot Andison, David Bird, Murchison Callender, Melanie Campbell, Vivian Choh, Michael Doughty, Teresa Hildebrand, Howard Howland, Elizabeth Irving, Jerome Kuszak, Collette Lebert, Kelley Moran, Brian Levy, Jack Pasternak, Joram Piatigorsky, Lorne Ryall, Ruth Pickett-Seltner, Michelle Pardue, Sandra Priolo, Olga Vrablic, Judy West, Judy Weerheim, and Sophia Zaidi. Special thanks are given to Kelley Moran and Vladimir Bantseev. The author is grateful for many years of support from the Natural Sciences and Engineering Research Council of Canada (NSERC). 
Brewster D. On the structure of the crystalline lens in fishes and quadrupeds. Phil Trans R Soc. 1816.311–317.
Krogh A. The progress of physiology. Am J Physiol. 1929;90:243–251.
Hodgkin AL, Huxley AF. The components of membrane conductance in the giant axon of Loligo. J Physiol. 1952;116:473–496. [CrossRef] [PubMed]
Hartline HK, Wagner HG, Ratcliff F. Inhibition in the eye of Limulus. J Gen Physiol. 1956;39:651–673. [CrossRef] [PubMed]
Walls GL. The Vertebrate Eye and Its Adaptive Radiation. 1942;1–785. Cranbrook Institute of Science Bloomfield Hills, MI.
Sivak JG. Accommodation in vertebrates. Zadunaisky JA Dacson H eds. Current Topics in Eye Research. 1980;281–330. Academic Press New York.
Wald G. The distribution and evolution of visual systems. Florkin M Mason HS eds. Comparative Biochemistry. 1960 Sources of Free Energy. 1960;1:311–345. Academic Press New York.
Gehring WJ. The genetic control of eye development and its implications for the evolution of the various eye-types. Int J Dev Biol. 2002;46:65–73. [PubMed]
Packard A. Cephalods and fish: the limits of convergence. Biol Rev Camb Philos Soc. 1972;47:241–307. [CrossRef]
Land M. Molluscs. Ali MA eds. Photoreceptors and Vision in Invertebrates. 1984;699–725. Plenum Press New York.
Worgul BV. Lens. Jacobiec FA eds. Ocular Anatomy, Embryology and Teratology. 1982;355–389. Harper & Row Philadelphia.
Sivak JG. Optical variability of the fish lens. Douglas RH Djamgoz MBA eds. The Visual System of Fish. 1990;63–80. Chapman & Hall London.
Meinertzhagen IA. Development of the squid’s visual system. Gilbert DL Adelman WJ, Jr Arnold JM eds. Squid as Experimental Animals. 1990;399–419. Plenum Press New York.
West JA, Sivak JG, Doughty MJ. Microscopical evaluation of the crystalline lens of the squid (Loligo opalescens) during embryonic development. Exp Eye Res. 1995;60:19–35. [CrossRef] [PubMed]
West JA, Sivak JG, Pasternak J, Piatigorsky J. Immunolocalization of S crystallins in the developing squid (Loligo opalescens) lens. Dev Dyn. 1994;199:85–92. [CrossRef] [PubMed]
Sivak JG. Shape and focal properties of the cephalopod ocular lens. Can J Zool. 1991;69:2501–2506. [CrossRef]
Sivak JG, West JA, Campbell MC. Growth and optical development of the ocular lens of the squid (Sepioteuthis lessoniana). Vision Res. 1994;34:2177–2187. [CrossRef] [PubMed]
Wallace WC. Discovery of a muscle in the eye of fishes. Am J Sci Arts. 1834;26:394.
Andison ME, Sivak JG. The functional morphology of the retractor lentis muscle of a teleost fish, Astronotus ocellatus. Can J Zool. 1994;72:1880–1886. [CrossRef]
Beer T. Die Accommodation des Fischauges. Pflugers Arch Physiol. 1894;58:523–650. [CrossRef]
Somiya H, Tamura T. Studies on the visual accommodation in fishes. Jpn J Ichthyol. 1973;20:193–206.
Somiya H. Dynamic mechanism of visual accommodation in fishes: structure of the lens muscle and its nerve control. Proc R Soc London B Biol Sci. 1987;230:77–91. [CrossRef]
Meader RG. The innervation of the muscle of accommodation in the eye of the teleost Holocentrus. J Morphol. 1936;59:163–172. [CrossRef]
Sivak JG. Interrelation of feeding behaviour and accommodative lens movements in some species of North American freshwater fishes. J Fish Res Bd Can. 1973;30:1141–1146. [CrossRef]
Munk O. On the occurrence of two lens muscles in within each eye of some teleosts. Vidensk Medd Dan Naturhist Foren. 1971;134:7–19.
Pronek N. Oscars. 1982; TFH Publications Neptune City, NJ.
Sivak JG, Howland HC. Accommodation in the northern rock bass (Ambloplites rupestris rupestris) in response to natural stimuli. Vision Res. 1973;13:2059–2064. [CrossRef] [PubMed]
Andison ME, Sivak JG. The naturally-occurring accommodative response of the oscar, Astronotus ocellatus, to visual stimuli. Vision Res. 1996;36:3021–3027. [CrossRef] [PubMed]
Tamura T, Wisby WJ. The visual sense of pelagic fishes especially the visual axis and accommodation. Bull Marine Sci Gulf Caribbean. 1963;133:443–448.
Fernald RD, Wright SE. Growth of the visual system in the African cichlid fish Haplochromis burtoni: accommodation. Vision Res. 1985;25:163–170. [CrossRef] [PubMed]
Toates FM. Accommodation function of the human eye. Physiol Rev. 1972;52:828–863. [PubMed]
Daum KM. Accommodative response. Eskridge JB Amos J Bartlett JD eds. Clinical Procedures in Optometry. 1991;677–687. JB Lippincott Philadelphia.
Meyer DB. The avian eye and its adaptations. Crescitelli F eds. Handbook of Sensory Physiology. 1977 The Visual System of Vertebrates. 1977;VII/5:549–611. Springer-Verlag Berlin.
West JA, Sivak JG, Doughty MJ. Functional morphology of lenticular accommodation in the young chicken (Gallus domesticus). Can J Zool. 1991;69:2183–2193. [CrossRef]
Sivak JG, Vrablic OE. Ultrastructure of intraocular muscles of diving and non-diving ducks. Can J Zool. 1982;60:1588–1606. [CrossRef]
Martin AR, Pilar G. Dual mode of synaptic transmission in the avian ciliary ganglion. J Physiol. 1963;168:443–463. [CrossRef] [PubMed]
Levy B, Sivak JG. Mechanisms of accommodation in the bird eye. J Comp Physiol. 1980;137:267–272. [CrossRef]
Sivak JG, Hildebrand T., Lebert C. Magnitude and rate of accommodation in diving and non-diving birds. Vision Res. 1985;25:925–933. [CrossRef] [PubMed]
Glasser A, Howland HC. In vitro changes in back vertex distance chick and pigeon lenses: species differences and the effect of aging. Vision Res. 1995;35:1813–1824. [CrossRef] [PubMed]
Tripathi RC. Comparative physiology and anatomy of the outflow pathway. Davson H Graham LT eds. The Eye. 1974 Comparative Physiology. 1974;5:279–293. Academic Press New York.
Pardue MT, Sivak JG. The functional anatomy of the ciliary muscle in four avian species. Brain, Behavior Evol. 1996;49:295–311.
Kuszak JR, Sivak JG, Weerheim JA. Lens optical quality is a direct function of lens sutural architecture. Invest Ophthalmol Vis Sci. 1991;32:2119–2129. [PubMed]
Sivak JG, Herbert KL, Peterson KL, Kuszak JR. The inter-relationships of lens anatomy and optical quality. I. Non-primate lenses. Exp Eye Res. 1994;59:505–520. [CrossRef] [PubMed]
Kuszak JR, Peterson KL, Sivak JG, Herbert KL. The inter-relationship of lens anatomy and optical quality. II. Primate lenses. Exp Eye Res. 1994;59:521–535. [CrossRef] [PubMed]
Priolo S, Sivak JG, Kuszak JR. Effect of age on the morphology and optical quality of the avian crystalline lens. Exp Eye Res. 1999;69:629–640. [CrossRef] [PubMed]
Glasser A, Murphy CJ, Troilo D, Howland, HC. The mechanism of lenticular accommodation in chicks. Vision Res. 1995;35:1525–1540. [CrossRef] [PubMed]
Choh V, Meriney SD, Sivak JG. A physiological model to measure effects of age on lenticular accommodation and spherical aberration in chickens. Invest Ophthalmol Vis Sci. 2002;43:92–98. [PubMed]
Pardue M, Sivak JG. Age-related changes in human ciliary muscle. Optom Vis Sci. 2000;77:204–210. [CrossRef] [PubMed]
Farnsworth PN, Shyne SE. Anterior zonular shifts with age. Exp Eye Res. 1979;28:292–297.
Pardue M. Functional Anatomy of the Ciliary Muscle in Birds and Humans. Dissertation . 1996; University of Waterloo Waterloo, Ontario Canada.
Wallman J, Turkel J, Trachtman, J. Extreme myopia produced by modest changes in visual experience. Science. 1978;201:1249–1251. [CrossRef] [PubMed]
Wiesel TN, Raviola E. Myopia and eye enlargement after neonatal lid fusion in monkeys. Nature. 1977;266:66–68. [CrossRef] [PubMed]
Lauber JK, McGinnis J, Boyd J. The influence of mitotics, diamox and vision occluders on light-induced buphthalmus in domestic fowl. Proc Soc Exp Biol Med. 1965;120:572–575. [CrossRef] [PubMed]
Schaeffel F, Glasser A, Howland HC. Accommodation, refractive error and eye growth in chickens. Vision Res. 1988;28:639–657. [CrossRef] [PubMed]
Irving EL, Callender MG, Sivak JG. Inducing myopia, hyperopia and astigmatism in chicks. Optometry Vis Sci. 1991;68:364–368. [CrossRef]
Irving EL, Sivak JG, Callender MG. Refractive plasticity of the developing chick eye. Ophthalmic Physiol Opt. 1992;12:448–456. [CrossRef] [PubMed]
Irving EL, Callender MG, Sivak JG. Inducing ametropias in hatchling chicks by defocus: effect of aperture size, shape and cylindrical lenses. Vision Res. 1995;35:1165–1174. [CrossRef] [PubMed]
Hendrickson P, Rosenblum W. Accommodation demand and deprivation in kitten ocular development. Invest Ophthalmol Vis Sci. 1985;26:343–349. [PubMed]
Nathan J, Crewther SG, Crewther DP, Kiely PM. Effects of retinal image degradation on ocular growth in cats. Invest Ophthalmol Vis Sci. 1984;25:1300–1306. [PubMed]
Troilo D, Gottlieb MD, Wallman J. Visual deprivation causes myopia in chicks with optic nerve section. Curr Eye Res. 1987;6:993–999. [CrossRef] [PubMed]
Sivak JG, Ryall LA, Weerheim J, Campbell MCW. Optical constancy of the chick lens during pre and post-hatching ocular development. Invest Ophthalmol Vis Sci. 1989;30:967–974. [PubMed]
Pickett-Seltner RL, Weerheim J, Sivak JG, Pasternak JJ. Experimentally induced myopia does not affect post-embryonic development of the chick lens. Vision Res. 1987;27:1779–1782. [CrossRef] [PubMed]
Priolo S, Sivak JG, Kuszak JR, Irving EL. Effect of experimentally induced ametropia on the morphology and optical quality of avian crystalline lens. Invest Ophthalmol Vis Sci. 2000;41:3516–3522. [PubMed]
Zaidi S, Senchyna M, Sivak JG. Quantification of chick lens alpha A and delta crystallins in experimentally induced ametropia. Mol Vis. 2002;8:472–476. [PubMed]
Donders FC. On the Anomalies of Accommodation and Refraction of the Eye. 1864;343. The New Sydenham Society London.
von Helmholtz H. Treatise on Physiological Optics. 1909; 3rd ed. Verlag von Leopold Voss Hamburg, Germany. Translated by Southhall JPC. New York: Dover Publications; 1962:379
Wildsoet C, Wallman J. Choroidal and scleral mechanisms of compensation for spectacle lenses in chicks. Vision Res. 1995;35:1175–1194. [CrossRef] [PubMed]
Choh VCP. A Physiological Model to Measure Optical and Biophysical Changes during Avian Accommodation. Dissertation . 2001; University of Waterloo Waterloo, Ontario, Canada.
Choh V, Sivak JG, Irving EL, Wong W. Ultrasound biomicroscopy of the anterior segment of the enucleated chicken eye during accommodation. Ophthalmic Physiol Opt. 2002;22:401–408. [CrossRef] [PubMed]
Walter HE, Sayles LP. Biology of the Vertebrates. 1969; Macmillan New York.
Andison ME, Sivak JG, Bird DM. The refractive development of the eye of the American Kestrel (Falco sparverius): a new animal model. J Comp Physiol. 1992;170:565–574.
Figure 1.
 
Photograph of a 6.0-mm diameter glass sphere in water refracting parallel helium-neon laser beams of two separations. The difference in focal lengths of the two separations showing positive (or undercorrected) spherical aberration, reflects the homogeneous refractive index of the sphere.
Figure 1.
 
Photograph of a 6.0-mm diameter glass sphere in water refracting parallel helium-neon laser beams of two separations. The difference in focal lengths of the two separations showing positive (or undercorrected) spherical aberration, reflects the homogeneous refractive index of the sphere.
Figure 2.
 
Photograph of a 6.0-mm diameter fish lens (rock bass, Ambloplites rupestris) in physiological solution refracting parallel helium-neon laser beams of two separations. The lack of a difference in focal length of the two separations is indicative of the absence of spherical aberration due to the developmentally related gradient refractive index.
Figure 2.
 
Photograph of a 6.0-mm diameter fish lens (rock bass, Ambloplites rupestris) in physiological solution refracting parallel helium-neon laser beams of two separations. The lack of a difference in focal length of the two separations is indicative of the absence of spherical aberration due to the developmentally related gradient refractive index.
Figure 3.
 
Accommodative stimulus-response functions for humans (left) (adapted, with permission, from Toates FM. Accommodation function of the human eye. Physiol Rev. 1972;52:828–863. © American Physiological Society. First appeared in Meas Control. 1972;5:58–61. © IEEE) and (right) a fish, the oscar (Astronotus ocellatus) (adapted, with permission, from Andison ME, Sivak JG. The naturally-occurring accommodative response of the oscar, Astronotus ocellatus, to visual stimuli. Vision Res. 1996;36:3021–3027. © Elsevier), showing similar accommodative lag and lead. Left and right: x-axis: stimulus (in diopters); y-axis: response (in diopters).
Figure 3.
 
Accommodative stimulus-response functions for humans (left) (adapted, with permission, from Toates FM. Accommodation function of the human eye. Physiol Rev. 1972;52:828–863. © American Physiological Society. First appeared in Meas Control. 1972;5:58–61. © IEEE) and (right) a fish, the oscar (Astronotus ocellatus) (adapted, with permission, from Andison ME, Sivak JG. The naturally-occurring accommodative response of the oscar, Astronotus ocellatus, to visual stimuli. Vision Res. 1996;36:3021–3027. © Elsevier), showing similar accommodative lag and lead. Left and right: x-axis: stimulus (in diopters); y-axis: response (in diopters).
Figure 4.
 
Scanning electron micrographs of the anterior sutures of 7-day, 2-year-old and 5-year-old chicken lenses (main lens body without annular pad) showing age-related spread in the “point” suture. The white bar (bottom right) represents 100 μm while the black lines outline the extent of the suture area (reprinted, with permission, from Priolo S, Sivak JG, Kuszak JR. Effect of age on the morphology and optical quality of the avian crystalline lens. Exp Eye Res. 1999;69:629–640. © Academic Press.).
Figure 4.
 
Scanning electron micrographs of the anterior sutures of 7-day, 2-year-old and 5-year-old chicken lenses (main lens body without annular pad) showing age-related spread in the “point” suture. The white bar (bottom right) represents 100 μm while the black lines outline the extent of the suture area (reprinted, with permission, from Priolo S, Sivak JG, Kuszak JR. Effect of age on the morphology and optical quality of the avian crystalline lens. Exp Eye Res. 1999;69:629–640. © Academic Press.).
Figure 5.
 
Loss of lenticular amplitude of accommodation with age in chickens as measured using an in situ physiological model in which the ciliary nerve is stimulated (reprinted, with permission, from Choh V, Meriney SD, Sivak JG. A physiological model to measure effects of age on lenticular accommodation and spherical aberration in chickens. Invest Ophthalmol Vis Sci. 2002;43:92–98. © Cadmus Professional Communications).
Figure 5.
 
Loss of lenticular amplitude of accommodation with age in chickens as measured using an in situ physiological model in which the ciliary nerve is stimulated (reprinted, with permission, from Choh V, Meriney SD, Sivak JG. A physiological model to measure effects of age on lenticular accommodation and spherical aberration in chickens. Invest Ophthalmol Vis Sci. 2002;43:92–98. © Cadmus Professional Communications).
×
×

This PDF is available to Subscribers Only

Sign in or purchase a subscription to access this content. ×

You must be signed into an individual account to use this feature.

×