Nasotemporal asymmetry during teleost retinal growth: preserving an area of specialization

Teleost fish retinas grow throughout adult life through both cell addition and stretching. Cell division occurs at the periphery of the retina, resulting in annular addition of all cell types except rod photoreceptors, which are added in the central retina. Since many teleosts have a region of high cellular density at the temporal pole of the eye, we analyzed whether and how this specialized region of high visual acuity maintained its relative topographical position through asymmetric circumferential growth. To do this, we measured the pattern of long‐term retinal growth in the African cichlid Haplochromis burtoni. We found that the retina expands asymmetrically along the nasotemporal axis, with the nasal retina growing at a higher rate than the temporal, dorsal, or ventral retinae, whose growth rates are equal. This nasotemporal asymmetry is produced via significantly greater expansion of retinal tissue at the nasal pole rather than through differential cell proliferation. The mechanisms responsible for this differential retinal enlargement are unknown; however, such asymmetric expansion very likely minimizes disruption in vision during rapid growth. © 1999 John Wiley & Sons, Inc. J Neurobiol 41: 435–442, 1999     

Evidence for a driving role of ingrowing axons for the shifting of older retinal terminals in the tectum of fish

In amphibians and teleosts, retina and tectum grow incongruently. In order to maintain the retinotopy of the retinotectal projection, Gaze, Keating, and Chung (1974) postulated a shifting of terminals throughout growth. In order to test the possibility that ingrowing retinal fibers are the driving force for this shifting, we induced a permanent retinal projection into the ipsilateral tectum in juveniles of the cichlid fish Haplochromis burtoni. The surface of the tectum had increased (11–18 months later) 2.5–5.8 times, and the surface of the retina 8.6–14 times. Filling of ganglion cells with horseradish peroxidase (HRP) retrogradely from the tectum showed ipsilaterally regenerating ganglion cells only in the center of the retina. The position of ganglion cells indicated that the ipsilateral projection derived only from axotomized and regenerating retinal ganglion cells but not from those newly born. Ipsilaterally projecting retinal fibers showed terminals only in the rostral half of the tectum. Comparison of area of terminations of ipsilaterally projecting ganglion cells at various times after the crush provided no evidence for expansion or a shift into caudal tectal areas throughout the period of growth. These findings are compatible with the idea that newly ingrowing fibers induce older terminals to move caudally.     

Ocular dimensions and cone photoreceptor topography in adult Nile Tilapia <Emphasis Type="Italic">Oreochromis niloticus</Emphasis>

Information on the anatomy of the eye and the topography of cone photoreceptor cells in the retina is presented for the Nile Tilapia (Oreochromis niloticus). In adults, the shape and proportions of the ocular components of the prominent eye conform to the general form of fish eyes, as determined using cryo-sectioned eyes. The lens is approximately spherical and there is little variation in the distance from the centre of the lens to the border between the choroid and retina at a range of angles about the optical axis. The average ratio of the distance from the centre of the lens to the retina: lens radius (Matthiessen’s ratio) is 2.44:1. In retinal wholemounts, single and double (twin) cone photoreceptors, forming a square mosaic, are present. Peak photoreceptor densities for both morphological cone types are found in the temporal retina. Using peak cone densities and estimates of focal length from cryo-sectioned eyes, visual acuity is calculated to be 5.44 cycles per deg. The lack of apparent specific ocular or retinal specializations and the relatively low visual acuity reflect the lifestyle of the Nile Tilapia and may allow it to adapt to changes in visual environment in its highly variable natural habitat as well as contributing to the ‘ecological flexibility’ of this species.     

The lens controls cell survival in the retina: Evidence from the blind cavefish Astyanax

The lens influences retinal growth and differentiation during vertebrate eye development but the mechanisms are not understood. The role of the lens in retinal growth and development was studied in the teleost Astyanax mexicanus, which has eyed surface-dwelling (surface fish) and blind cave-dwelling (cavefish) forms. A lens and laminated retina initially develop in cavefish embryos, but the lens dies by apoptosis. The cavefish retina is subsequently disorganized, apoptotic cells appear, the photoreceptor layer degenerates, and retinal growth is arrested. We show here by PCNA, BrdU, and TUNEL labeling that cell proliferation continues in the adult cavefish retina but the newly born cells are removed by apoptosis. Surface fish to cavefish lens transplantation, which restores retinal growth and rod cell differentiation, abolished apoptosis in the retina but not in the RPE. Surface fish lens deletion did not cause apoptosis in the surface fish retina or affect RPE differentiation. Neither lens transplantation in cavefish nor lens deletion in surface fish affected retinal cell proliferation. We conclude that the lens acts in concert with another optic component, possibly the RPE, to promote retinal cell survival. Accordingly, deficiency in both optic structures may lead to eye degeneration in cavefish.     

Guanine and its retinal distribution in the tapetum of the bigeye tuna,thunnus obesus

The eye of the bigeye tuna (Thunnus obesus) contains a retinal tapetum composed of guanine. The total amount of the guanine in one eye of the fish (SL=120 cm) was about 88.6 mg. The mean guanine content of the tapetum was approximately 1.25 mg/cm² of the retinal surface. The highest content of guanine (2.15 mg/cm²) was observed only in the ventro-temporal part of the retina. To distinguish this area from the rest of the eye, we suggested the term ‘locus tapetalis’ for it. The visual accommodation system clearly indicated that the visual axis of the fish is upper-forward and the resulting retinal area for acute vision was suggested to be in the ventro-temporal retina. We discussed that the area centralis of the bigeye tuna may have two functions: to guarantee high visual acuity and to allow for high photo-sensitivity in dim light vision.     

Nasotemporal asymmetry during teleost retinal growth: preserving an area of specialization.

Teleost fish retinas grow throughout adult life through both cell addition and stretching. Cell division occurs at the periphery of the retina, resulting in annular addition of all cell types except rod photoreceptors, which are added in the central retina. Since many teleosts have a region of high cellular density at the temporal pole of the eye, we analyzed whether and how this specialized region of high visual acuity maintained its relative topographical position through asymmetric circumferential growth. To do this, we measured the pattern of long-term retinal growth in the African cichlid Haplochromis burtoni. We found that the retina expands asymmetrically along the nasotemporal axis, with the nasal retina growing at a higher rate than the temporal, dorsal, or ventral retinae, whose growth rates are equal. This nasotemporal asymmetry is produced via significantly greater expansion of retinal tissue at the nasal pole rather than through differential cell proliferation. The mechanisms responsible for this differential retinal enlargement are unknown; however, such asymmetric expansion very likely minimizes disruption in vision during rapid growth.     

Retinal Anatomy of hatchling sea turtles: Anatomical specializations and behavioral correlates

The eyes of three species of sea turtle hatchlings (loggerheads, green turtles, and leatherbacks) possess visual streaks, areas of densely packed ganglion cells running along the antero‐posterior retinal axis. These probably function to provide heightened visual acuity along the horizon. The vertical extent and absolute concentration of cells within the streak, compared to the rest of the retina, differ among the species. Leatherbacks have an additional specialized region (area temporalis) that might enhance their ability to detect prey below them in the water column. Green turtles and loggerheads, but not leatherbacks, show compensatory eye reflexes that keep the visual streak horizontal. Species differences in retinal structure and eye reflexes probably reflect their unique specializations in visual ecology and behaviour.     

Guanine-type retinal tapetum and ganglion cell topography in the retina of a carangid fish, Kaiwarinus equula.

A guanine-type retinal tapetum was recorded in the eyes of a carangid fish Kaiwarinus equula (= Carangoides equula), spectrophotometric evidence of such being presented. The total amount of guanine in one eye was about 6.5 mg, the guanine density being ca. 1.3 mg cm(-2) over the retinal surface area. To examine the guanine distribution within the retina, the latter was divided into 21 regions. An area of high guanine density (more than 2.0 mg cm(-2)) was observed in the dorsal fundus of the retina, suggesting that the most sensitive vision was checked downward. Using whole-mount retinal preparations, the distribution of Nissl-stained cells within the retinal ganglion cell layer was examined. The greatest cell density area (area centralis) was observed only in the temporal retina. The visual acuity of the area centralis was 4.3 cycles deg(-1), suggesting that high resolution and binocular vision were directed frontally in this species. The eyes of a related carangid (Pseudocaranx dentex), lacking a tapetum, were also examined for comparison. The possible ecological advantage resulting from the tapetum is discussed in terms of visual threshold.     

Retinal ganglion cell topography and spatial resolution in the smelt Hypomesus japonicus (Brevoort, 1856)

The present study deals with the topography of retinal ganglion cells (GCs) and spatial resolution in the smelt Hypomesus japonicus. The eyes and retinae were examined by light microscopy and computerized tomography. DAPI labelling was used to visualize cell nuclei in the ganglion cell and inner plexiform layers. Two zones of increased GC density in the nasal and temporal retina were bridged by a horizontal streak with the GC density ranging from 5600 to 8000 cells/mm². The maximum cell density (area retinae temporalis) ranged from 9492 to 14,112 cells/mm², and the total number of GCs varied from 286 x 10³ to 326 x 10³ cells in three individuals. The theoretical anatomical spatial resolution (the anatomical estimate of the upper limit of visual acuity) was minimum in the ventral periphery (smaller fish, 1.43 cpd; larger fish, 1.37 cpd) and maximum in area retinae temporalis (smaller fish, 2.83 cpd; larger fish, 2.41 cpd). The relatively high density of GCs and presence of the horizontal streak and area retinae temporalis in the H. japonicus are consistent with its highly visual behaviour. The present findings contribute to better understanding of the factors affecting the topography of retinal ganglion cells and mechanisms of visual adaptation in fish.     

Evidence for a driving role of ingrowing axons for the shifting of older retinal terminals in the tectum of fish.

In amphibians and teleosts, retina and tectum grow incongruently. In order to maintain the retinotopy of the retinotectal projection, Gaze, Keating, and Chung (1974) postulated a shifting of terminals throughout growth. In order to test the possibility that ingrowing retinal fibers are the driving force for this shifting, we induced a permanent retinal projection into the ipsilateral tectum in juveniles of the cichlid fish Haplochromis burtoni. The surface of the tectum had increased (11-18 months later) 2.5-5.8 times, and the surface of the retina 8.6-14 times. Filling of ganglion cells with horseradish peroxidase (HRP) retrogradely from the tectum showed ipsilaterally regenerating ganglion cells only in the center of the retina. The position of ganglion cells indicated that the ipsilateral projection derived only from axotomized and regenerating retinal ganglion cells but not from those newly born. Ipsilaterally projecting retinal fibers showed terminals only in the rostral half of the tectum. Comparison of area of terminations of ipsilaterally projecting ganglion cells at various times after the crush provided no evidence for expansion or a shift into caudal tectal areas throughout the period of growth. These findings are compatible with the idea that newly ingrowing fibers induce older terminals to move caudally.     

Retinal ganglion cell topography and visual acuity of the sleepy lizard (<Emphasis Type="Italic">Tiliqua rugosa</Emphasis>)

The spatial distribution of retinal ganglion cells provides valuable insight into the importance species place on observing objects in specific regions of their visual field with higher spatial resolving power. We estimate the total number, distribution and peak density of ganglion cells in retinal wholemounts of the sleepy lizard, Tiliqua rugosa, a scincid lizard endemic to southern Australia. Ganglion cells were readily discernable from amacrine cells by their size and shape, prominent nuclei and the accumulation of Nissl-positive substances in their cytoplasm. A total of 1,654,200 (±59,400) presumed ganglion cells were estimated throughout the retina, distributed irregularly and forming a loose horizontal streak of high cell density peaking at 15,500 cells per mm². With a post nodal distance of 6.25 mm, we calculate an upper limit of visual acuity of 6.8 c/deg.     

Effects of retinal dopamine depletion on the growth of the fish eye

We investigated the suitability of fishes as animal models to study the involvement of the retinal dopaminergic system in the visually guided control of eye growth (emmetropization). Advantages of such a model system are (i) that all dopaminergic cells in the retina can be destroyed without apparent damage to other neurons, (ii) simple optical design and short depth of field of the eye, and (iii) continuous growth throughout life. Depleting the retina of dopamine in Aequidens pulcher (Cichlidae) had no apparent effect on refractive state, since size and focal length of the eye were reduced by the same amount. Furthermore, imposed defocus was compensated at a normal rate in spite of the absence of retinal dopamine. In A. pulcher, the dopaminergic system of the retina thus appears not to have an essential role in emmetropization. Our results furthermore suggest that in eyes of more complicated optical design, manipulation of the retinal dopaminergic system may lead to unrelated effects indistinguishable from direct interference with emmetropization. A major disadvantage of the fish model was that refractive state of the eye could not be measured accurately in vivo with standard methods. Accepted: 9 January 1999     

Gdf6a is required for the initiation of dorsal–ventral retinal patterning and lens development

Dorsal–ventral patterning of the vertebrate retina is essential for accurate topographic mapping of retinal ganglion cell (RGC) axons to visual processing centers. Bone morphogenetic protein (Bmp) growth factors regulate dorsal retinal identity in vertebrate models, but the developmental timing of this signaling and the relative roles of individual Bmps remain unclear. In this study, we investigate the functions of two zebrafish Bmps, Gdf6a and Bmp4, during initiation of dorsal retinal identity, and subsequently during lens differentiation. Knockdown of zebrafish Gdf6a blocks initiation of retinal Smad phosphorylation and dorsal marker expression, while knockdown of Bmp4 produces no discernable retinal phenotype. These data, combined with analyses of embryos ectopically expressing Bmps, demonstrate that Gdf6a is necessary and sufficient for initiation of dorsal retinal identity. We note a profound expansion of ventral retinal identity in gdf6a morphants, demonstrating that dorsal BMP signaling antagonizes ventral marker expression. Finally, we demonstrate a role for Gdf6a in non-neural ocular tissues. Knockdown of Gdf6a leads to defects in lens-specific gene expression, and when combined with Bmp signaling inhibitors, disrupts lens fiber cell differentiation. Taken together, these data indicate that Gdf6a initiates dorsal retinal patterning independent of Bmp4, and regulates lens differentiation.     

Ontogenetic changes in retinal structure and visual acuity: a comparative study of coral-reef teleosts with differing post-settlement lifestyles

Changes in retinal structure during settlement were investigated in four species of tropical reef-associated teleost fishes with differing periods of planktonic duration and post-settlement lifestyles. They were: Apogon doederleini (Apogonidae), a nocturnal planktivore; Stethojulis strigiventer (Labridae), a diurnal microcarnivore; Upeneus tragula (Mullidae), a carnivore which uses chin barbels to disturb invertebrates from the sediment; and Pomacentrus moluccensis (Pomacentridae), a diurnal herbivorous planktivore. The densities of cones, rods, cells in the inner nuclear layer and cells in the ganglion cell layer were estimated in a size range of each species. Visual acuity was calculated using cone densities and lens diameter. The ontogenetic sequence of changes in cell density was similar in all species but interspecific variation in the timing and rates of change was found and could be related to lifestyle. For example, cone densities decreased and rod densities increased most rapidly in the nocturnal species, A. doederleini, during settlement. In contrast, high cone densities were maintained in the species adopting a diurnal lifestyle. Theoretical visual acuity was found to increase rapidly as lens size increased, but was similar for all species at similar lens sizes, indicating the importance of larger eye size as a means for improving resolution during early stages of eye growth. It was concluded that for the species undergoing abrupt lifestyle changes at settlement, structural re-organisation of the retina is important for the survival of the fish as they leave the pelagic environment and take up their reef-associated lifestyle.     

The position of the retinal area centralis changes with age in Champsocephalus gunnari (Channichthyidae), a predatory fish from coastal Antarctic waters

Histological examinations of the topographical distribution and the area of highest density (the area centralis: AC) of presumed retinal ganglion cells found in the retina in 0- to 6-year-old Champsocephalus gunnari revealed differences between younger and older fish. Individuals of up to 2 years of age had the AC in the temporal retina, whereas in 3-, 4-, 5- and 6-year-old fish it was positioned in the ventro-temporal region of the retina. The main visual axis in the pitch plane of C. gunnari was shown to shift from facing forward to an upward-forward direction during growth, corresponding to the habitat change in this species from pelagic to benthic. Moreover, the AC in 0- to 3-year-old fish was near the retinal periphery, but displaced towards the inner retina in 4- to 6-year-old fish. This means that the visual axis in the horizontal plane of the younger fish was directed towards the frontal sector of vision, while in the older fish a slightly more lateral position was favoured. Therefore, younger fish can be expected to possess superior binocular vision when it comes to prey closely in front of them, but in older fish it seems more important to have a wider visual field to detect prey (and possibly predators) within a greater volume of water.     

Regressive evolution: ontogeny and genetics of cavefish eye rudimentation

Two hypotheses exist to explain ontogenetic eye reduction in Astyanax cave fish: first, after lens induction by the primordial eye cup, the lens plays the role of a central regulator of eye and retina regression or, second, the retina itself is an independent unit of eye development. A comparative study of five blind cave fish populations and their surface sister form was performed to investigate the differences of ontogenetic eye regression between the cave populations during different stages of development. The study revealed that, in addition to the initial formation of smaller primordia, eye regression is also caused during later ontogeny by different relative growth and specific histological characteristics. Whereas the cave fish lens never properly differentiates, the regressive process of the retina is transitorily interrupted by ongoing differentiation. In the newly-discovered Molino cave population, even visual cells with well-organized outer segments develop, which are secondarily reduced at a later ontogenetic stage. This result shows that the retina and lens are independent developmental units within the eye ball. Presumably, the genetic systems responsible for both show independent inheritance, which is also corroborated by hybrids of F ₂-crosses between the cave and surface fish, in which lens and retina development do not correlate. During ontogeny, the eye size differs between the cave populations. In Pachón cave fish, the relatively large eye size correlates with an ancient introgression from a surface population, which may have delayed eye regression.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 287–296.     

Retinal topography of ganglion cells in immature ocean sunfish, <Emphasis Type="Italic">Mola mola</Emphasis>

The ocean sunfish, Mola mola, is the largest known bony fish. Based on prior studies of diet composition, it is considered to be a pelagic zooplanktivore. However, a recent study using acoustic telemetry revealed that they repeatedly dive to depths of >50 m during the day. We examined the distribution of cells within the retinal ganglion cell layer in the immature ocean sunfish (c.a. 50 cm total length) and estimated their visual acuity with respect to the main visual axis and visual fields. Visual acuity was between 3.37 and 4.41 cycles/degree. The region of highest cell density was located in the dorso-temporal retina, indicating that the main visual axis of ocean sunfish is directed towards the lower frontal portion of the visual field. This axis is considered beneficial for detecting prey items when the sunfish are migrating vertically through the water column, and in foraging behavior near the sea bottom.     

Apoptosis of the mammalian retina and lens

Although retinal neurons usually last the entire lifetime of an individual, many innate genetic and developmental errors and external stimuli can reduce their longevity leading to loss of visual acuity or blindness. Similarly, the lens, largely composed of denucleated fiber cells must remain transparent for life if vision is to remain clear. Apoptosis of retinal neurons and newly generated lens fiber cells contributes to retinal degeneration and cataract formation, respectively, in both humans and experimental mammals. The apoptosis is triggered by many stimuli in addition to inherited mutations and may be amenable to pharmacologic amelioration. These studies not only provide new clinical insights but also the opportunity to investigate the molecular pathways leading to apoptosis in an organ that is not required for survival. The eye, becomes, therefore, an important organ for evaluation of theories of apoptosis in vivo.     

Peculiarities of the eye morphology and the spectral sensitivity of the retinal photoreceptors of the Pacific saury <Emphasis Type="Italic">Cololabis saira</Emphasis>

This study examines some peculiarities of the eye organization and spectral properties of retinal photoreceptors of the Pacific saury Cololabis saira. The saury has relatively large eyes with a developed accomodation apparatus and an area of enhanced visual acuity (the fovea) in the retina. A specialized pigmented septum is observed in the vitreal cavity, which is supposed to function as a light-shading screen. The retina contains numerous rods and single and double cones arranged in a square mosaic pattern. Microspectrophotometric measurements indicated that their max occurs at 502 (rods), 380 (single cones), and 478/565 (double cones) nm. Such properties can provide color vision in a broad spectral range, including UV light. The peripheral visual apparatus of the Pacific saury is typical of active diurnal predatory fish that inhabit shallow and upper pelagic water layers.     

Ocular changes accompanying eye loss in the spider family uloboridae

In uloborid spiders, eye loss is accompanied by increased visual angles, optical material investment, and potential visual acuity of the retained eyes. Relative to carapace volume, the six-eyed Hyptiotes cavatus and two four-eyed Miagrammopes species have greater retinal hemisphere areas and lens volumes than do the eight-eyed uloborids Waitkera waitkerensis, Uloborus glomosus, and Octonoba sinensis. In Waitkera, in which the eyes have little visual overlap, and in Miagrammopes, in which eye loss simplifies the spiders' patterns of visual overlap, increased retinal cell density enhances potential visual acuity. However, this occurs at the expense of potential retinal cell sensitivity.