Loss of Active Neurogenesis in the Adult Shark Retina

Neurogenesis is the process by which progenitor cells generate new neurons. As development progresses neurogenesis becomes restricted to discrete neurogenic niches, where it persists during postnatal life. The retina of teleost fishes is thought to proliferate and produce new cells throughout life. Whether this capacity may be an ancestral characteristic of gnathostome vertebrates is completely unknown. Cartilaginous fishes occupy a key phylogenetic position to infer ancestral states fixed prior to the gnathostome radiation. Previous work from our group revealed that the juvenile retina of the catshark Scyliorhinus canicula, a cartilaginous fish, shows active proliferation and neurogenesis. Here, we compared the morphology and proliferative status of the retina in catshark juveniles and adults. Histological and immunohistochemical analyses revealed an important reduction in the size of the peripheral retina (where progenitor cells are mainly located), a decrease in the thickness of the inner nuclear layer (INL), an increase in the thickness of the inner plexiform layer and a decrease in the cell density in the INL and in the ganglion cell layer in adults. Contrary to what has been reported in teleost fish, mitotic activity in the catshark retina was virtually absent after sexual maturation. Based on these results, we carried out RNA-Sequencing (RNA-Seq) analyses comparing the retinal transcriptome of juveniles and adults, which revealed a statistically significant decrease in the expression of many genes involved in cell proliferation and neurogenesis in adult catsharks. Our RNA-Seq data provides an excellent resource to identify new signaling pathways controlling neurogenesis in the vertebrate retina.

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Loss of active neurogenesis in the adult shark retina

10.1101/2020.11.19.389973 ◽

2020 ◽

Author(s):

Ismael Hernández-Núñez ◽

Diego Robledo ◽

Hélène Mayeur ◽

Sylvie Mazan ◽

Laura Sánchez ◽

...

Keyword(s):

Cell Proliferation ◽

Progenitor Cells ◽

Peripheral Retina ◽

Postnatal Life ◽

Teleost Fishes ◽

Rna Seq ◽

Scyliorhinus Canicula ◽

Plexiform Layers ◽

Active Proliferation ◽

Excellent Resource

AbstractNeurogenesis is the process by which progenitor cells generate new neurons. As development progresses neurogenesis becomes restricted to concrete neurogenic niches, where it persists during postnatal life. The retina of teleost fishes is thought to proliferate and produce new cells throughout life. Whether this capacity may be an ancestral characteristic of jawed vertebrates, shared with chondrichthyans, which diverged from osteichthyans prior to the gnathostome radiation is completely unknown. Previous work from our group revealed that the juvenile retina of the catshark Scyliorhinus canicula shows active proliferation and neurogenesis. Here, we compared the morphology and proliferative status of the retina between catshark juveniles and adults. Histological analyses revealed an important reduction in the size of the peripheral retina (where progenitor cells are mainly located), an increase in the thickness of the plexiform layers and a decrease in the thickness of the inner nuclear layer in adults. Contrary to what has been reported in teleost fish, we did not observe active mitotic activity in the catshark retina after sexual maturation, suggesting that there is no significant proliferation and neurogenesis in adult specimens. Based on these results, we carried out RNA-Sequencing (RNA-Seq) analyses comparing the retinal transcriptome of juveniles and adults, which revealed a statistically significant decrease in the expression of many genes involved in cell proliferation and neurogenesis in adult catsharks. Our RNA-Seq data provides an excellent resource to identify new signaling pathways controlling neurogenesis in the vertebrate retina.

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The morphology and topographic distribution of substance- P-like immunoreactive amacrine cells in the cat retina

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1989.0060 ◽

1989 ◽

Vol 237 (1289) ◽

pp. 471-488 ◽

Cited By ~ 28

Keyword(s):

Substance P ◽

Ganglion Cell ◽

Plexiform Layer ◽

Amacrine Cells ◽

Maximum Density ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Cat Retina ◽

Area Centralis ◽

Topographic Distribution

In cat retinal wholemounts, substance-P-like immunoreactivity (SP-IR) was localized in a distinct population of amacrines whose cell bodies were normally placed in the ganglion cell layer. Although displaced amacrines accounted for 80-95% of the SP-IR amacrines in peripheral retina, this proportion decreased considerably within the area centralis, accounting for 50-80% of the labelled cells at maximum density. The SP-IR cells in both the inner nuclear and ganglion cell layers gave rise to well-defined varicose dendrites of uniform appearance that stratified around 60% depth (S3/S4) of the inner plexiform layer. In addition, sparse fine dendrites in stratum 1 (S1) could sometimes be traced to inner nuclear cells and occasionally to displaced amacrines. The combined SP-IR cell density ranged from less than 50 cells mm -2 in the far periphery to more than 500 cells mm -2 in the area centralis; the maximum density showed little individual variation despite wide differences in the proportion of displaced cells. The 39000 SP-IR amacrines in a mapped retina had a triangular topographic distribution, with intermediate isodensity lines extending vertically in superior retina and horizontally along both arms of the visual streak. Colocalization experiments established that all SP-IR cells in cat retina showed GABA-like immunoreactivity, and that the SP-IR amacrines were quite distinct from the cholinergic amacrines identified by choline acetyltransferase immunohistochemistry.

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Rod bipolar cells in the cone-dominated retina of the tree shrew Tupaia belangeri

Visual Neuroscience ◽

10.1017/s0952523800002625 ◽

1991 ◽

Vol 6 (6) ◽

pp. 629-639 ◽

Cited By ~ 21

Author(s):

Brigitte Müller ◽

Leo Peichl

Keyword(s):

Bipolar Cell ◽

Tree Shrew ◽

Light And Electron Microscopy ◽

Plexiform Layer ◽

Bipolar Cells ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Cat Retina ◽

Topographical Distribution ◽

Rod Bipolar Cells

AbstractThe tree shrew has a cone-dominated retina with a rod proportion of 5%, in contrast to the common mammalian pattern of rod-dominated retinae. As a first step to elucidate the rod pathway in the tree shrew retina, we have demonstrated the presence of rod bipolar cells and studied their morphology and distribution by light and electron microscopy.Rod bipolar cells were labeled with an antiserum against the protein kinase C (PKC), a phosphorylating enzyme. Intense PKC immunoreactivity was found in perikarya, axons, and dendrites of rod bipolar cells. The cell bodies are located in the sclerad part of the inner nuclear layer, the dendrites ascend to the outer plexiform layer where they are postsynaptic to rod spherules, and an axon descends towards the inner plexiform layer (IPL). The axons branch, and terminate in the vitread third of the IPL where mammalian rod bipolar cells are known to terminate. Two amacrine cell processes are always seen as the postsynaptic elements (dyads). Dendritic and axonal arbors of rod bipolar cells are rather large, up to 100 μm in diameter. The topographical distribution of the rod bipolar cells was analyzed quantitatively in tangential sections.Their density ranges from 300 cells/mm2 in peripheral retina to 900 cells/mm2 more centrally. The distribution is rather flat with no local extremes. Consistent with the low rod proportion in tree shrew, the rod bipolar cell density is low compared to the rod-dominated cat retina for example (36,000-47,000 rod bipolar cells/mm2). Rod-to-rod bipolar cell ratios in the tree shrew retina range from smaller than 1 to about 7, and thus are also lower than in cat.

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Development of morphological types and distribution patterns of amacrine cells immunoreactive to tyrosine hydroxylase in the cat retina

Visual Neuroscience ◽

10.1017/s0952523800002315 ◽

1990 ◽

Vol 4 (02) ◽

pp. 159-175 ◽

Cited By ~ 28

Author(s):

Hou-Hua Wang ◽

Nicolas Cuenca ◽

Helga Kolb

Keyword(s):

Cell Body ◽

Total Population ◽

Amacrine Cell ◽

Plexiform Layer ◽

Amacrine Cells ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Cat Retina

AbstractUsing an antibody against tyrosine hydroxylase on newborn to 30-day kitten retinas, we have been able to follow the development of the dopaminergic amacrine cells of the cat retina by light-microscopical investigations of retinal wholemounts. The Type 1 or large Toh+ amacrine cells described by others (Oyster et al., 1985; Törk & Stone, 1979) and named A18 from a Golgi study (Kolb et al., 1981), is at birth (P1) an immature neuron with a small cell body and two or three simple thick radiating dendrites stratifying in stratum 1 with many of the dendrites ending in enlarged growth cones. With increasing postnatal age, the cell body size increases from 12.5 μm diameter to reach 15.5 μm diameter at P30. The dendritic fields also increase in size and complexity. At P1, cells of the central area exhibit dendritic appendages which then develop progressively until at P13 (after eye opening) they are part of rudimentary rings and by P30 the dendritic plexus of Toh+ dendrites and rings in stratum 1, typical of the adult cells, are complete. Toh+ stained processes with growth cones that run deep in stratum 5 of the inner plexiform layer and processes passing to the outer plexiform layer first become apparent at P1 in cells of central inferior retina but not till after P13 are these processes clearly expressed. At P1, the total number of Toh+ Type 1 cells is approximately 4000 and this number remains unchanged to the adult retina. However, the retina increases in size over the Pl–P30 stage and thus the mean density of Type 1 Toh+ cells decreases from 30/mm2at P1 to 18/mm2at P30. The maximum density of Type 1 Toh+ cells occurs in central retina 2–4 mm superior temporal to the area centralis, corresponding to the maximum rod photoreceptor concentration.A second type of small Toh+ amacrine cell can be visualized at P1. This Type 2 cell is characterized by a much smaller cell body than Type 1 cells (9 μm diameter), and with faintly stained dendrites located in stratum 3 of the inner plexiform layer. During later postnatal days, Type 2 cells gradually become unstainable and only few are still seen in far peripheral retina by P23. Type 2 Toh+ cells form a total population of 40,000 cells at P1 with their highest density occurring in peripheral retina. By P13, they cannot be seen in central retina and are reduced to a total population of cells staining for the antibody of 7400 cells in far peripheral retina. Their density decreases from 233/mm2at P1 to 0/mm2at P30. The transiently staining population of Type 2 Toh+ immunoreactive cells probably correspond to the small THI-CA-cell seen in rat retina (Nguyen–Legros et al., 1983), and the second type of dopaminergic amacrine cell seen in macaque retina (Mariani & Hokoc, 1988).

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Development of glutamate receptor subunit 2 immunoreactivity in postnatal rat retina

Visual Neuroscience ◽

10.1017/s0952523800175078 ◽

2000 ◽

Vol 17 (5) ◽

pp. 737-742 ◽

Cited By ~ 5

Author(s):

KJELL JOHANSSON ◽

ANITHA BRUUN ◽

MARIE TÖRNGREN ◽

BERNDT EHINGER

Keyword(s):

Ganglion Cell ◽

Glutamate Receptor ◽

Ganglion Cells ◽

Plexiform Layer ◽

Outer Plexiform Layer ◽

Postnatal Life ◽

Inner Plexiform Layer ◽

Protein Levels ◽

Subunit Expression ◽

Cell Somata

Previous studies have shown that the expression of glutamate receptor subunits is developmentally regulated and have been implicated in processes of cell differentiation during postnatal life. The tissue localization and developmental pattern of the glutamate receptor 2 subunit of the α-amino-3-hydroxy-5-methyl-4-isoxazoleproprionate (AMPA) receptor were investigated by means of immunohistochemistry and immunoblotting. Labeling of amacrine and ganglion cells and the inner plexiform layer appeared early during development, while glutamate receptor 2 subunit expression in the outer plexiform layer started after the first postnatal week. The distribution of labeling within the inner plexiform layer changed from nonorganized to laminated appearance prior to eye-opening. There was an increasing number of positive amacrine and ganglion cell somata during the first 2 weeks, but their number decreased considerably as the retina matured and were seen at least up to 35 days of postnatal development. Little labeling was found in the ganglion cell layer and in the inner plexiform layer of late postnatal and adult retina. Labeling in the outer plexiform layer and of bipolar cell somata appeared to increase in the developing retina. Glur2 labeling of these cells and the outer plexiform layer became discernible during the second postnatal week, and this labeling was present in the adult as well. Immunoblotting showed that GluR2 protein levels were similar at postnatal days 7 and 10, but slightly decreased between the second and fourth postnatal weeks. Our data imply that the immunological expression of glutamate receptor 2 subunit in the inner plexiform layer decreases as a function of age, and is correlated with developmental event(s) in the postnatal retina.

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Cholecystokinin-like immunoreactive amacrine cells in the rat retina

Visual Neuroscience ◽

10.1017/s0952523802194156 ◽

2002 ◽

Vol 19 (4) ◽

pp. 531-540 ◽

Cited By ~ 7

Author(s):

SALLY I. FIRTH ◽

CAROLINA VARELA ◽

PEDRO DE LA VILLA ◽

DAVID W. MARSHAK

Keyword(s):

Cellular Localization ◽

Plexiform Layer ◽

Amacrine Cells ◽

Cell Types ◽

Bipolar Cells ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Rat Retina ◽

Rats And Mice ◽

Rod Bipolar Cells

High levels of endogenous cholecystokinin (CCK) are present in the rat retina (Eskay & Beinfeld, 1982), but the cellular localization and physiological actions of CCK in the rat retina are uncertain. The goals of this study were to characterize the cells containing CCK, identify cell types that interact with CCK cells, and investigate the effects of CCK on rod bipolar cells. Rat retinas were labeled with antibody to gastrin-CCK (gCCK) using standard immunofluorescence techniques. Patch-clamp methods were used to record from dissociated rod bipolar cells from rats and mice. Gastrin-CCK immunoreactive (-IR) axons were evenly distributed throughout the retina in stratum 5 of the inner plexiform layer of the rat retina. However, the gCCK-IR somata were only detected in the ganglion cell layer in the peripheral retina. The gCCK-IR cells contained glutamate decarboxylase, and some of them also contained immunoreactive substance P. Labeled axons contacted PKC-IR rod bipolar cells, and recoverin-IR ON-cone bipolar cells. CCK-octapeptide inhibits GABAC but not GABAA mediated currents in dissociated rod bipolar cells.

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The morphological characterization and distribution of displaced ganglion cells in the anuran retina

Visual Neuroscience ◽

10.1017/s0952523800009883 ◽

1989 ◽

Vol 3 (6) ◽

pp. 551-561 ◽

Cited By ~ 7

Author(s):

Pál Tóth ◽

Charles Straznicky

Keyword(s):

Optic Nerve ◽

Ganglion Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Cell Types ◽

Dendritic Morphology ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Retinal Position ◽

Retinal Distribution

AbstractThe number, dendritic morphology, and retinal distribution of displaced ganglion cells were studied in two anuran species, Xenopus laevis and Bufo marinus. Horseradish peroxidase or cobaltic lysine complex was applied to the cut end of the optic nerve, and the size, shape, and retinal position of retrogradely filled ganglion cells displaced into the inner nuclear layer were determined in retinal wholemount and sectioned material. Approximately 1% of ganglion cells in Xenopus and 0.1% in Bufo were found to be displaced. In both species, many of the previously described orthotopic ganglion cell types (Straznicky & Straznicky, 1988; Straznicky et al., 1990) were present among displaced ganglion cells. In Xenopus more displaced ganglion cells were found in the retinal periphery than in the retinal center, and they formed 3 or 4 distinct bands around the optic nerve head. In Bufo the incidence of displaced ganglion cells was higher along the visual streak than in the dorsal and ventral peripheral retina. These results indicate that the distribution of displaced ganglion cells approximates the retinal distribution of orthotopic ganglion cells. One of the likely mechanisms to account for this developmental paradox may be that the formation of the inner plexiform layer, adjacent to the ciliary margin, acts as a mechanical barrier by preventing the entry of some of the late developing ganglion cells into the ganglion cell layer.

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The DAPI-3 amacrine cells of the rabbit retina

Visual Neuroscience ◽

10.1017/s0952523800012141 ◽

1997 ◽

Vol 14 (3) ◽

pp. 473-492 ◽

Cited By ~ 39

Author(s):

Layne L. Wright ◽

Colin L. Macqueen ◽

Guy N. Elston ◽

Heather M. Young ◽

David V. Pow ◽

...

Keyword(s):

Ganglion Cells ◽

Dendritic Tree ◽

Plexiform Layer ◽

Amacrine Cells ◽

Dendritic Morphology ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Rabbit Retina ◽

High Level ◽

Cholinergic Amacrine Cells

AbstractIn the rabbit retina, the nuclear dye, 4,6, diarnidino-2-phenylindole (DAPI), selectively labels a third type of amacrine cell, in addition to the previously characterized type a and type b cholinergic amacrine cells. In this study, these “DAPI-3” amacrine cells have been characterized with respect to their somatic distribution, dendritic morphology, and neurotransmitter content by combining intracellular injection of biotinylated tracers with wholemount immunocytochemistry. There are about 100,000 DAPI-3 amacrine cells in total, accounting for 2% of all amacrine cells in the rabbit retina, and their cell density ranges from about 130 cells/mm2 in far-peripheral retina to 770 cells/mm2 in the visual streak. The thin varicose dendrites of the DAPI-3 amacrine cells form a convoluted dendritic tree that is symmetrically bistratified in S1/S2 and S4 of the inner plexiform layer. Tracer coupling shows that the DAPI-3 amacrine cells have a fivefold dendritic-field overlap in each sublamina, with the gaps in the arborization of each cell being occupied by dendrites from neighboring cells. The DAPI-3 amacrine cells consistently show the strongest glycine immunoreactivity in the rabbit retina and they also accumulate exogenous [3H]-glycine to a high level. By contrast, the All amacrine cells, which are the best characterized glycinergic cells in the retina, are amongst the most weakly labelled of the glycine-immunopositive amacrine cells. The DAPI-3 amacrine cells costratify narrowly with the cholinergic amacrine cells and the On-Off direction-selective ganglion cells, suggesting that they may play an important role in movement detection.

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Presumptive catecholaminergic ganglion cells in the pigeon retina

Visual Neuroscience ◽

10.1017/s0952523800003370 ◽

1990 ◽

Vol 4 (3) ◽

pp. 225-235 ◽

Cited By ~ 17

Author(s):

Kent T. Keyser ◽

Luiz R. G. Britto ◽

Jong-Inn Woo ◽

Dong H. Park ◽

Tung H. Joh ◽

...

Keyword(s):

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Peripheral Retina ◽

Inner Plexiform Layer ◽

Central Retina ◽

The Difference ◽

Pigeon Retina ◽

Rate Limiting ◽

Two Populations

AbstractAn antiserum directed against tyrosine hydroxylase (TH), the rate-limiting enzyme in the synthesis of dopamine, was used to study the pigeon retina. Labeled cells were observed in both the inner nuclear layer (INL) and ganglion cell layer (GCL). Two populations of TH-immunoreactive neurons were observed in the INL. Some of these cells were 7−10 μ in diameter and gave rise to processes that arborized in three Layers of the inner plexiform layer (IPL). These cells appeared similar to the dopaminergic amacrine cells described previously (Marc, 1988). Other labeled cells in the INL were 12−20 μ in diameter and were recognizable as a previously described subpopulation of TH-immunoreactive displaced ganglion cells (Britto et al., 1988).A population of labeled cells was observed in the GCL. Counts of these cells in two retinae revealed 5000 and 7000 cells, respectively. They ranged in size from 8−15 μ in diameter in the central retina and from 8−20 m in diameter in the peripheral retina. The density of labeled cells was highest in the central retina and red field and lowest in the retinal periphery. The difference in cell size and cell density as a function of eccentricity is characteristic of the total population of ganglion cells in the avian retina (Ehrlich, 1981; Hayes, 1982). Some of the TH-positive cells in the GCL could be classified as ganglion cells for two reasons: (1) The axons of many of the TH-positive cells in the GCL were TH-immunoreactive as well and could be followed to the optic nerve head. (2) The injection of rhodamine-labeled microspheres into the nucleus geniculatus lateralis, pars ventralis (GLv), resulted in the retrograde labeling of many of the TH-positive cells in the contralateral retina.

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Inner Retinal Morphology and Visual Outcomes in Idiopathic Epiretinal Membrane Surgery: A Retrospective Optical Coherence Tomography Study

Journal of VitreoRetinal Diseases ◽

10.1177/2474126421989614 ◽

2021 ◽

pp. 247412642198961

Author(s):

Ioannis S. Dimopoulos ◽

Michael Dollin

Keyword(s):

Optical Coherence Tomography ◽

Epiretinal Membrane ◽

Strong Predictor ◽

Plexiform Layer ◽

Inner Plexiform Layer ◽

Optical Coherence ◽

Visual Outcomes ◽

Retinal Pathology

Purpose: Epiretinal membrane (ERM) is a common retinal finding for patients older than 50 years. Disorganization of the retinal inner layers (DRIL) has emerged as a novel predictor of poor visual acuity (VA) in eyes with inner retinal pathology. The aim of our study is to correlate preoperative DRIL with visual outcomes after ERM surgery. Methods: Medical records and optical coherence tomography (OCT) images of 81 pseudophakic patients who underwent treatment of idiopathic ERM were reviewed. Preoperative DRIL on OCT was correlated with VA at baseline and at 3 and 6 months after ERM surgery. DRIL was defined as the loss of distinction between the ganglion cell–inner plexiform layer complex, inner nuclear layer, and outer plexiform layer. DRIL severity was based on its extent within the central 2-mm region of a transfoveal B-scan (absent/mild: <one-third, severe: >one-third horizontal width). Results: Review of preoperative OCT showed severe DRIL in 41% and absent/mild DRIL in 59%. Severe DRIL was associated with worse baseline VA ( P < .001). Preoperative VA and DRIL status at baseline were both predictors of postoperative VA at follow-up time points ( P < .001). Severe DRIL was associated with significantly less improvement in VA at 6 months (–0.23 logMAR for absent/mild vs –0.14 for severe DRIL). Conclusions: Presence of severe preoperative DRIL correlates with worse baseline VA in patients with ERM and reduced VA improvement at 6 months. DRIL can be a strong predictor of long-term poor visual outcomes in ERM surgery.

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