Retinal histogenesis and cell differentiation in an elasmobranch species, the small‐spotted catshark Scyliorhinus canicula (original) (raw)
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Variation in the development of fish retina
Although the basic structure of the vertebrate retina is similar across taxa, high variability in specific features of the fish retina reflects the differences in visual microhabitat of these species. The vertebrate retina is the first step in the neural integration of visual information. A great deal of retinal function can be inferred from structure, and as these relationships continue to be revealed, we are gaining new insights into how vision is integrated by the nervous system. Among fishes, the developmental rate and acquisition of retinal structures is highly variable. While some species develop all structures early in embryogenesis, others delay acquisition of the full adult retinal complement of cells until months after hatching. Given the tight relationship between structure and function, differences in the timing of retinogenesis have implications for the visionbased survival skills of the early life history stages and for the overall ecology and fitness of the species. Although much of the observed variation may be related to altricial versus precocial life history strategies, we suggest that protracted retinal development also reflects and separates the constraints imposed by the requirements of foraging and predator avoidance. As evidenced by a typically monochromatic all-cone retina, the eye of early fish larvae is adapted for efficient foraging in bright light. At later stages, an improved ability to identify the presence of predators is acquired via addition of rod photoreceptors for low light vision, as well as multiple cone spectral channels (and regularly geometric cone mosaics) for increased contrast and motion sensitivity. The larval retina of some species exhibits further specializations, such as the pure rod retina of the eel leptocephalus and the pure green cone retina of many marine teleosts. Overall, variation in the development of the teleost retina can be viewed as a continuum from very rapid to greatly delayed. The developmental trajectory of the visual system in any given species represents a product of evolutionary history, developmental constraints, and foraging and predation pressures.
Variation in the development of the fish retina
by the American Fisheries Society V V V V Variation in the Dev ariation in the Dev ariation in the Dev ariation in the Dev ariation in the Development of the F elopment of the F elopment of the F elopment of the F elopment of the Fish Retina ish Retina ish Retina ish Retina ish Retina Abstract.—Although the basic structure of the vertebrate retina is similar across taxa, high variabil-ity in specific features of the fish retina reflects the differences in visual microhabitat of these species. The vertebrate retina is the first step in the neural integration of visual information. A great deal of retinal function can be inferred from structure, and as these relationships continue to be revealed, we are gaining new insights into how vision is integrated by the nervous system. Among fishes, the developmental rate and acquisition of retinal structures is highly variable. While some species develop all structures early in embryogenesis, others delay acquisition of the full adult retinal ...
Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas
Journal of Chemical Neuroanatomy, 2010
We studied the pattern of cell proliferation and its relation with photoreceptor differentiation in the embryonic and postembryonic retina of two elasmobranchs, the lesser spotted dogfish (Scyliorhinus canicula) and the brown shyshark (Haploblepharus fuscus). Cell proliferation was studied with antibodies raised against proliferating cell nuclear antigen (PCNA) and phospho-histone-H3, and early photoreceptor differentiation with an antibody raised against rod opsin. As regards the spatiotemporal distribution of PCNA-immunoreactive cells, our results reveal a gradual loss of PCNA that coincides in a spatiotemporal sequence with the gradient of layer maturation. The presence of a peripheral growth zone containing pure-proliferating retinal progenitors (the ciliary marginal zone) in the adult retina matches with the general pattern observed in other groups of gnathostomous fishes. However, in the shark retina the generation of new cells is not restricted to the ciliary marginal zone but also occurs in retinal areas that contain differentiated cells: (1) in a transition zone that lies between the pureproliferating ciliary marginal zone and the central (layered) retina; (2) in the differentiating central area up to prehatching embryos where large amounts of PCNA-positive cells were observed even in the inner and outer nuclear layers; (3) and in the retinal pigment epithelium of prehatching embryos. Rod opsin immunoreactivity was observed in both species when the outer plexiform layer begins to be recognized in the central retina and, as we previously observed in trout, coincided temporally with the weakening in PCNA labelling.
Developmental Brain Research, 2005
We have analyzed the patterns of cell proliferation and cell death in the retina and optic tectum of the brown trout (Salmo trutta fario) throughout embryonic and postembryonic stages. Cell proliferation was detected by immunohistochemistry with an antibody against the proliferating cell nuclear antigen (PCNA), and apoptosis by means of the TUNEL method. Haematoxylin and DAPI staining were also used to demonstrate apoptotic cells. Photoreceptor cell differentiation was assessed by immunohistochemistry with antibodies against opsins. Throughout embryonic development, PCNA-immunoreactive (PCNA-ir) cells become progressively restricted to the peripheral growth zone of the retina, which appears to be the principal source of new retinal cells from late embryos to adults. However, some PCNA-ir cells are observed secondarily in the differentiated retina, first in the inner nuclear layer of 15-mm alevins and later in the outer nuclear layer of 16-mm alevins, after differentiation of the first rods in the central retina, as demonstrated with opsin immunocytochemistry. Our observations also support the view that the PCNA-ir cells observed secondarily in the INL of the central retina of alevins are photoreceptor precursors. The number and distribution of apoptotic cells in the retina and optic tectum of the trout change throughout development, allowing distinction of several waves of apoptosis. Cell death is detected in proliferating areas at early stages, then in postmitotic or differentiating areas, and later concurring temporal and spatially with the establishment of visual circuits, thus indicating a relationship between apoptosis and proliferation, differentiation and synaptogenesis. D
Emergence and development of immunoreactive cells in teleostean retinas during the perinatal period
Developmental Brain Research, 1990
We have used light-microscopical immunoh,stochemlstry to invest,gate developmental changes of several neurochemical indicators in retinas of perlnatal kllhflsh and goldfish Immunoreactlve prohferatlng cell nuclear ant,gen (,r-PCNA/cychn, a marker for rephcatIng cells) was present in nucle~ of all neuroblasts m the early monolayer stage, but was lost progresswelv m central-to-peripheral and proximal-to-distal order as the layers and cells of the mature retina appeared The loss of ,r-PCNA was slightly prior to the appearance of lr-TH (tyrosine hydroxylase), GAD (glutamlc acid decarboxylase) and GS (glutamme synthetase) at the 4th embryonic day (E4) in both fish Since hatching was earlier m goldfish (E5) than in kllhflsh (E7), neurochemical maturation was evident at 2-3 days before hatching in kllhfish but not until around hatching In goldfish Two markers, lr-somatostatm and protein klnase C, were detected by the 1st postnatal day (H1) in goldfish, but not m permatal or adult kllhfish retinas Thus the course of development of kllhfish and goldfish retinas is similar, but not identical The vahdlty of Ir-PCNA as a marker for proliferating cells is confirmed by the comodence of its disappearance with the appearance of neurochem,cal markers for mature, postmltot,c retinal cells
… Zoology Part B: …, 2010
We describe the major events in the retinogenesis in an altricial fish species, the Senegalese sole. The major developmental events in the sole retina occurred early after hatching (posthatching day 0, P0). Thus, (1) plexiform layers became recognizable at P1. (2) Proliferative activity disappeared from the central retina at P1, and, as development progressed, became restricted to cells located in the circumferential germinal zone, and to sparse cells dispersed throughout the inner nuclear layer and the outer nuclear layer. (3) Apoptotic cells were sparsely observed, randomly localized in all three nuclear layers of the early posthatching retina from P0 to P4. (4) The first synaptic vesicles were detected at P0 in early postmitotic ganglion cells. However, their appearance in the plexiform layers was delayed until P2. (5) The neurochemical development of most major retinal cell classes occurred between P0 and P5. Thus, although Isl1 immunoreactive ganglion cells were the first to become postmitotic in the vitreal surface of the central retina at P0, the first glutamine synthetase-expressing Müller cells appeared in the central retina by P5. The onset of expression for other retinal markers, such as rod opsin, calretinin, parvalbumin, a-tyrosine hydroxylase, and a-protein kinase C, occurred between P2 and P4. Our results suggest that the most relevant processes involved in Senegalese sole retinogenesis occur during the prolarval and early larval stages (P0-P5). Furthermore, we conclude that altricial fish species may constitute a convenient model organism to address the relationship between the structural and functional development of sensory organs with the acquisition of behavioral repertoires. Martín-Partido G, Francisco-Morcillo J. 2010. Eye development and retinal differentiation in an altricial fish species, the senegalese sole (Solea senegalensis, Kaup 1858). J. Exp. Zool. (Mol. Dev. Evol.) 314B:580-605.
Developmental Brain Research, 1983
Key words: retina --fish development --neuronal death --NOR development --retinopetal innervation -transcellular HRP-labelling Adult patterns and the development of the nucleus of origin of centrifugal innervation of the retina, the nucleus olfacto-retinalis (NOR), were studied with horseradish peroxidase in 2 cichlid fish species. In the adults large and small cells within the nuclear boundaries can be distinguished by their cytoarchitecture and their HRP-labelling. The NOR is already formed at hatching (5.5 days postspawning) but cannot be filled by HRP injections into one eye until 2 days later. The number of labelled neurons increases steadily until adult cell density is reached. Later larval stages show that the NOR neurons also increase in size. The two cell types found in the adult can first be distinguished at around 30 days post-spawning. Early unilateral enucleation reduces the density of the small cells in the contralateral NOR. In spite of different environmental constraints on the growth of the larvae, the NOR develops in a similar way in both species but always somewhat later in the substrate-spawner than in the mouth-brooder. The centrifugal innervation of bird (isthmo-optic nucleus, ION) and fish (NOR) retinae starts at comparable developmental stages of the retina, but no cell death as found in the developing ION in birds occurs in the developing NOR in fish. It is suggested that this is due to the constant adjustment of the NOR to the ever increasing cell numbers in the fish retina. The NOR is thus the only known centrifugally projecting nucleus in vertebrates which lacks extensive degenerating patterns during early development. The known LH-RH immunoreactivity, the two cell types, the early development, and the projection to the retina of the NOR in cichlid fish resemble closely characteristics of the ganglion of the terminalis nerve of other piscine species.
Morphological patterns in the developing vertebrate retina
Anatomy and Embryology, 1991
Changes in the morphology of the early optic cup were observed in embryos of two distantly-related vertebrate species, a teleost fish, northern pike (Esox lucius), and chicken (GalIus gallus). A similar morphological pattern was noted to appear in both species shortly after the involution of the optic vesicle and the formation of the inner retinal layer. At a gross level, three notches were observed in the retinal margin at approximately nasal, dorsal, and temporal positions, while in histological sections a sharp constriction was found in the thickness of the dorsal retinal layer. In both species, this dorsal constriction appeared to be continuous with the central or dorsal notch. The time of appearance and configuration of this morphological pattern is intriguingly similar to the specification and polarity of retinal positional markers, and suggest a segmentation hypothesis for the origin of retinal polarity.
Neuroscience, 2007
In the retina of many lower vertebrates, the arrangement of cells, in particular of cone photoreceptors, is highly regular. The data presented in this report show that in the retina of a cichlid fish (Astatotilapia burtoni) the regular arrangement is not restricted to cone photoreceptors and their synaptic terminals but can be found in elements of the inner retina as well. A variety of immunocytochemical and other markers was used in combination with confocal microscopy on whole-mount preparations and tangential sections. Nearest neighbor analysis was performed and density recovery profiles as auto-and cross-correlograms were generated. Cells displaying a regular arrangement of their synaptic processes in matching radial register to each other were identified for each major retinal neuronal cell type except ganglion cells (i.e. photoreceptors, horizontal cells, bipolar cells, and amacrine cells). The precise location of some of the corresponding cell bodies was not as regular but still non-random, however there was no spatial cross-correlation between cell bodies of different types. The radial processes of Müller glial cells displayed a distribution correlating to the arrangement of photoreceptors and neurons. Thus, for one Müller glial cell I found two PKC-positive cone bipolar cells, a spatially corresponding grid of parvalbumin-positive amacrine cell processes, one H1 horizontal cell, and two pairs of double cones. There was no evidence among ganglion cells matching this pattern, possibly due to the lack of suitable markers. Although many other cell types do not follow this matching regular mosaic arrangement, a basic columnar building block can be postulated for the retina at least in cichlid fish. This suggests a functional radial unit from photoreceptors to the inner plexiform layer.
Experimental eye …, 2010
The calcium-binding protein calretinin (CR) has been widely used as a marker of neuronal differentiation. In the present study we analyzed the distribution of CR-immunoreactive (CR-ir) elements in the embryonic and postembryonic retina of two elasmobranchs, the lesser spotted dogfish (Scyliorhinus canicula) and the brown shyshark (Haploblepharus fuscus). We compared the distribution of CR with that of a proliferation marker (the proliferating cell nuclear antigen, PCNA) in order to investigate the time course of CR expression during retinogenesis and explored the relationship between CR and glutamic acid decarboxylase (GAD), the synthesizing enzyme of the gamma-aminobutyric acid (GABA), which has been reported to play a role in shark retinogenesis. The earliest CR immunoreactivity was concurrently observed in subsets of: a) ganglion cells in the ganglion cell layer; b) displaced ganglion cells in the inner plexiform layer and inner part of the inner nuclear layer (INLi); c) amacrine cells in the INLi, and d) horizontal cells. This pattern of CR distribution is established in the developing retina from early stage 32, long after the appearance of a layered retinal organization in the inner retina, and coinciding with photoreceptor maturation in the outer retina. We also demonstrated that CR is expressed in postmitotic cells long after they have exited the cell cycle and in a subset of GABAergic horizontal cells. Overall our results provide insights into the differentiation patterns in the elasmobranch retina and supply further comparative data on the development of CR distribution in the retina of vertebrates. This study may help in understanding the possible involvement of CR in aspects of retinal morphogenesis.