scholarly journals Characterization and staging of outer plexiform layer development in human retina and retinal organoids

Development ◽  
2021 ◽  
Author(s):  
Sumitha Prameela Bharathan ◽  
Angela Ferrario ◽  
Kayla Stepanian ◽  
G. Esteban Fernandez ◽  
Mark W. Reid ◽  
...  
Keyword(s):  
Visual Processing ◽  
Spatial Organization ◽  
Protein Localization ◽  
Plexiform Layer ◽  
Staging System ◽  
Bipolar Cells ◽  
Outer Plexiform Layer ◽  
Human Retina ◽  
Fetal Retina

The development of the first synapse of the visual system between photoreceptors and bipolar cells in the outer plexiform layer (OPL) of the human retina is critical for visual processing but poorly understood. By studying the maturation state and spatial organization of photoreceptors, depolarizing bipolar cells, and horizontal cells in the human fetal retina, we establish a pseudo-temporal staging system for OPL development that we term OPL-Stages 0 to 4. This was validated through quantification of increasingly precise subcellular localization of Bassoon to the OPL with each stage (p<0.0001). By applying these OPL staging criteria to human retinal organoids (HROs) derived from human embryonic and induced pluripotent stem cells, we observed comparable maturation from OPL-Stage 0 at day 100 in culture up to OPL-Stage 3 by day 160. Quantification of presynaptic protein localization confirmed progression from OPL-Stage 0 to 3 (p<0.0001). Overall, this study defines stages of human OPL development through mid-gestation and establishes HROs as a model system that recapitulates key aspects of human photoreceptor-bipolar cell synaptogenesis in vitro.

Immunohistochemical analysis of the outer plexiform layer in the nob mouse shows no abnormalities

2003 ◽  
Vol 20 (3) ◽  
pp. 267-272 ◽  
Author(s):  
SHERRY L. BALL ◽  
MACHELLE T. PARDUE ◽  
MAUREEN A. MCCALL ◽  
RONALD G. GREGG ◽  
NEAL S. PEACHEY
Keyword(s):  
Expression Pattern ◽  
Signal Transmission ◽  
Plexiform Layer ◽  
Immunohistochemical Analysis ◽  
Bipolar Cells ◽  
Outer Plexiform Layer ◽  
Mouse Retina ◽  
Voltage Gated ◽  
Voltage Gated Calcium Channels ◽  
Immunohistochemical Techniques

In the nob mouse, a mutation in nyctalopin results in a loss of signal transmission from photoreceptors to depolarizing bipolar cells (DBCs). We used immunohistochemical techniques to assess the expression pattern of proteins found at either the photoreceptor terminal or bipolar cell dendrites within the outer plexiform layer. We labeled normal and nob retinas with antibodies against mGluR6, PKC, G0α, bassoon, PSD-95, the α1F subunit of voltage-gated calcium channels, trkB, and dystrophin. All labeling patterns in nob and normal retinas were comparable to those previously reported in mouse retina. Our results indicate that the absence of nyctalopin does not disrupt the expression pattern of other proteins known to be required for synaptic transmission.

Morphological differentiation of bipolar cells in the ferret retina

1999 ◽  
Vol 16 (6) ◽  
pp. 1133-1144 ◽  
Author(s):  
E.D. MILLER ◽  
M.N. TRAN ◽  
G.-K. WONG ◽  
D.M. OAKLEY ◽  
R.O.L. WONG
Keyword(s):  
Visual Processing ◽  
Plexiform Layer ◽  
Morphological Differentiation ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Axon Terminals ◽  
Ribbon Synapses ◽  
Rod Bipolar Cells ◽  
Cone Bipolar Cells ◽  
Dye Labeling

Bipolar cells are not only important for visual processing but input from these cells may underlie the reorganization of ganglion cell dendrites in the inner plexiform layer (IPL) during development. Because little is known about the development of bipolar cells, here we have used immunocytochemical markers and dye labeling to identify and follow their differentiation in the neonatal ferret retina. Putative cone bipolar cells were immunoreacted for calbindin and recoverin, and rod bipolar cells were immunostained for protein kinase C (PKC). Our results show that calbindin-immunoreactive cone bipolar cells appear at postnatal day 15 (P15), at which time their axonal terminals are already localized to the inner half of the IPL. By contrast, recoverin-immunoreactive cells with terminals in the IPL are present at birth, but many of these cells may be immature photoreceptors. By the second postnatal week, recoverin-positive cells resembling cone bipolar cells were clearly present, and with increasing age, two distinct strata of immunolabeled processes occupied the IPL. PKC-containing rod bipolar cells emerged by the fourth postnatal week and at this age have stratified arbors in the inner IPL. The early bias of bipolar axonal arbors in terminating in the inner or outer half of the IPL is confirmed by dye labeling of cells with somata in the inner nuclear layer. At P10, several days before ribbon synapses have been previously observed in the ferret IPL, the axon terminals of all dye-labeled bipolar cells were clearly stratified. The results suggest that bipolar cells could provide spatially localized interactions that are suitable for guiding dendritic lamination in the inner retina.

The Development of the Outer Plexiform Layer of the Mouse Retina

1972 ◽  
Vol 30 ◽  
pp. 56-57
Author(s):  
Janet C. Blanks ◽  
Anthony M. Adinolfi ◽  
Richard N. Lolley
Keyword(s):  
Electron Microscopy ◽  
Osmium Tetroxide ◽  
Adult Mouse ◽  
Light And Electron Microscopy ◽  
Plexiform Layer ◽  
Uranyl Acetate ◽  
Bipolar Cells ◽  
Outer Plexiform Layer ◽  
Mouse Retina ◽  
Lead Citrate

In the all-rod retina of the adult mouse, synaptic contacts in the outer plexiform layer occur between photoreceptor terminals and dendritic processes of horizontal and bipolar cells. The postnatal development of the outer plexiform layer has been studied by light and electron microscopy. Following decapitation and enucleation of the eyes, samples of retinae from DBA mice (newborn to fourteen days) were removed and fixed by immersion in solutions of buffered glutaraldehyde and paraformaldehyde. The tissue was postfixed in osmium tetroxide, dehydrated and embedded in araldite. Sections were stained with uranyl acetate and lead citrate.With light microscopy, the outer plexiform layer first appears in the central retina as a gap within the neuroblastic layer on the fifth postnatal day. The separation is completed by the seventh postnatal day and appears mature by the fourteenth postnatal day.

Roles of aspartate and glutamate in synaptic transmission in rabbit retina. I. Outer plexiform layer

1985 ◽  
Vol 53 (3) ◽  
pp. 699-713 ◽  
Author(s):  
S. A. Bloomfield ◽  
J. E. Dowling
Keyword(s):  
Plexiform Layer ◽  
Second Order ◽  
Bipolar Cells ◽  
Outer Plexiform Layer ◽  
Horizontal Cells ◽  
Diethyl Ester ◽  
Rabbit Retina ◽  
Lower Vertebrate ◽  
Rods And Cones ◽  
Low Concentrations

Intracellular recordings were obtained from horizontal and bipolar cells of the superfused, isolated retina-eyecup of the rabbit. The putative neurotransmitters aspartate, glutamate, and several analogues were added to the superfusate while the membrane potential and light-responsiveness of the retinal neurons were monitored. Both L-aspartate and L-glutamate mimicked the actions of the endogenous photoreceptor transmitter on horizontal cells, on-bipolar cells, and off-bipolar cells. At applied concentrations of 2.5-20 mM, the actions of L-aspartate and L-glutamate were indistinguishable. D-aspartate potentiated the effects of both L-aspartate and L-glutamate on horizontal cells. This suggests that active uptake systems for these amino acids exist in the outer plexiform layer (OPL) of the rabbit retina. The glutamate analogue kainate produced effects similar to those of aspartate and glutamate on second-order neurons, but at concentrations lower by over two orders of magnitude. The glutamate analogue quisqualate had effects similar to kainate but with much less potency. The aspartate analogue n-methyl DL-aspartate (NMDLA) antagonized the effects of the photoreceptor transmitter on horizontal and off-bipolar cells. This action of NMDLA was only observed at low concentrations (50 microM). In addition, NMDLA could block the effects of exogenously applied kainate. The NMDLA had no clear effects on on-bipolar cells. The glutamate analogue 2-amino-4-phosphonobutyrate reversibly blocked the responses of on-bipolar cells but had no effect on either horizontal or off-bipolar cell responses. This suggests that on-bipolar cells possess a unique synaptic receptor. The aspartate analogue 2-amino-3-phosphonoproprionate did not show this selectivity, suggesting that this unique receptor is a glutamate-preferring receptor. The antagonists alpha-methyl glutamate, alpha-amino adipate, and glutamate diethyl ester all showed only a weak ability to antagonize the actions of the photoreceptor transmitter on second-order neurons. The results of this study indicate that glutamate or a glutamate-like substance is the likely transmitter of rods and cones in the rabbit retina. A comparison of the present findings with those previously obtained in lower vertebrate retinas suggests that the basic pharmacological design of the OPL of all vertebrate retinas is very similar.

Synaptic connexions made by horizontal cells within the outer plexiform layer of the retina of the cat and the rabbit

1974 ◽  
Vol 186 (1085) ◽  
pp. 317-331 ◽  
Keyword(s):  
Horizontal Cell ◽  
Plexiform Layer ◽  
Cell Types ◽  
Bipolar Cells ◽  
Outer Plexiform Layer ◽  
Horizontal Cells ◽  
Chemical Synapses

Two ultrastructurally distinctive types of horizontal cells are described in the retinae of the cat and the rabbit. Evidence is presented that they have different synaptic connexions in the outer plexiform layer. The majority of the presynaptic structures identified in the outer plexiform layer of the rabbit (as defined on page 320) belong to a neurofilamentous type of horizontal cell. It is suggested that the cat may be the same. No synapses have been identified on to, or from, the second, predominantly neurotubular, type of horizontal cell. No chemical synapses on to, or between, horizontal cells have been found. Thus input of this kind to both types of horizontal cells is as yet only known to be from the photoreceptors. All positively identified postsynaptic processes were the dendrites or perikarya of bipolar cells. Other cell types that are possibly pre- or postsynaptic in the outer plexiform layer are discussed.

Differential staining of neurons in the human retina with antibodies to protein kinase C isozymes

1993 ◽  
Vol 10 (2) ◽  
pp. 341-351 ◽  
Author(s):  
Helga Kolb ◽  
Li Zhang ◽  
Laura Dekorver
Keyword(s):  
Protein Kinase C ◽  
Protein Kinase ◽  
Plexiform Layer ◽  
Bipolar Cells ◽  
Wide Field ◽  
Human Retina ◽  
Axon Terminals ◽  
Kinase C ◽  
Pkc Β ◽  
Cone Bipolar Cells

AbstractMonoclonal antibodies to the three isozymes of protein kinase C (PKC) (α, β, and γ) were applied to postmortem human retina. Immunostaining was done on wholemount, or cryostat-sectioned retina, and visualized after ABC/DAB procedures by light (LM) and electron (EM) microscopy.The PCK-α antibody stained rod bipolar cells throughout the retina. EM analysis confirmed they were PKC-α-immunoreactive (IR) on their characteristic dendritic and axonal synaptology. Putative blue cone bipolar cells with wide-field axon terminals, stratifying in s5 of the inner plexiform layer (IPL), were also PKC-α-IR, and EM showed them to engage in narrow-cleft ribbon junctions in blue cone pedicles.The PKC-β antibody stained cone bipolar cells, many amacrine cells, and most ganglion cells. Cone bipolar cells were stained all the way into the foveal center: both midget and diffuse varieties were included. The IPL was densely PKC-IR and individual neurons could not be identified on stratification patterns. EM of the outer plexiform layer (OPL) revealed that both flat and invaginating cone bipolar types were IR and that IR axon terminals were presynaptic in all strata of the IPL. The occurrence of PKC-β-IR bipolar axons in stratum 2 of the IPL suggests that OFF-center as well as ON-center types were included.The PKC-γ antibody gave inferior staining compared with results from the other two antibodies; however, two varieties of wide-field monostratified amacrine cell and a large-bodied ganglion cell type were discernible.PKC in one form or another appears to be a second messenger used in neurotransmission by both rod and cone systems and ON- and OFF-center systems in the human retina.

scholarly journals Differential encoding of spatial information among retinal on cone bipolar cells

2015 ◽  
Vol 114 (3) ◽  
pp. 1757-1772 ◽  
Author(s):  
Robert J. Purgert ◽  
Peter D. Lukasiewicz
Keyword(s):  
Parallel Processing ◽  
Visual Processing ◽  
Amacrine Cell ◽  
Spatial Information ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Spatial Tuning ◽  
Cone Bipolar Cells

The retina is the first stage of visual processing. It encodes elemental features of visual scenes. Distinct cone bipolar cells provide the substrate for this to occur. They encode visual information, such as color and luminance, a principle known as parallel processing. Few studies have directly examined whether different forms of spatial information are processed in parallel among cone bipolar cells. To address this issue, we examined the spatial information encoded by mouse ON cone bipolar cells, the subpopulation excited by increments in illumination. Two types of spatial processing were identified. We found that ON cone bipolar cells with axons ramifying in the central inner plexiform layer were tuned to preferentially encode small stimuli. By contrast, ON cone bipolar cells with axons ramifying in the proximal inner plexiform layer, nearest the ganglion cell layer, were tuned to encode both small and large stimuli. This dichotomy in spatial tuning is attributable to amacrine cells providing stronger inhibition to central ON cone bipolar cells compared with proximal ON cone bipolar cells. Furthermore, background illumination altered this difference in spatial tuning. It became less pronounced in bright light, as amacrine cell-driven inhibition became pervasive among all ON cone bipolar cells. These results suggest that differential amacrine cell input determined the distinct spatial encoding properties among ON cone bipolar cells. These findings enhance the known parallel processing capacity of the retina.

Anatomical pathways for color vision in the human retina

1991 ◽  
Vol 7 (1-2) ◽  
pp. 61-74 ◽  
Author(s):  
Helga Kolb
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cells ◽  
Horizontal Cell ◽  
Plexiform Layer ◽  
Outer Plexiform Layer ◽  
Inner Plexiform Layer ◽  
Human Retina ◽  
Cell Responses ◽  
Single Cone ◽  
Section Electron

AbstractThe major neurons and neural circuits that are involved in the transmission of color signals through the human retina to produce the color and spatially opponent P cell or midget ganglion cell responses are described. The older findings of single cone to midget bipolar connectivity is reviewed, and the single midget bipolar cell to midget ganglion cell connectivity as revealed by a recent serial section electron microscope study is described in detail. Our present knowledge concerning the discrimination of the blue-cone subtype from the other longer wavelength cones in the human at the outer plexiform layer is summarized, and our most recent findings concerning horizontal cell connectivity to the different spectral types of cones are discussed. Finally, a hypothetical pathway is proposed for color-opponent surrounds of midget ganglion cells using both horizontal cells at the outer plexiform layer and amacrine cell pathways at the inner plexiform layer.

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