Melanopsin and calbindin immunoreactivity in the inner retina of humans and marmosets

2019 ◽  
Vol 36 ◽  
Author(s):  
Ashleigh J. Chandra ◽  
Sammy C.S. Lee ◽  
Ulrike Grünert
Keyword(s):  
Ganglion Cell ◽  
Calcium Binding ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Human Retina ◽  
Immunohistochemical Markers ◽  
Starburst Amacrine Cells

Abstract In primate retina, the calcium-binding protein calbindin is expressed by a variety of neurons including cones, bipolar cells, and amacrine cells but it is not known which type(s) of cell express calbindin in the ganglion cell layer. The present study aimed to identify calbindin-positive cell type(s) in the amacrine and ganglion cell layer of human and marmoset retina using immunohistochemical markers for ganglion cells (RBPMS and melanopsin) and cholinergic amacrine (ChAT) cells. Intracellular injections following immunolabeling was used to reveal the morphology of calbindin-positive cells. In human retina, calbindin-labeled cells in the ganglion cell layer were identified as inner and outer stratifying melanopsin-expressing ganglion cells, and ON ChAT (starburst amacrine) cells. In marmoset, calbindin immunoreactivity in the ganglion cell layer was absent from ganglion cells but present in ON ChAT cells. In the inner nuclear layer of human retina, calbindin was found in melanopsin-expressing displaced ganglion cells and in at least two populations of amacrine cells including about a quarter of the OFF ChAT cells. In marmoset, a very low proportion of OFF ChAT cells was calbindin-positive. These results suggest that in both species there may be two types of OFF ChAT cells. Consistent with previous studies, the ratio of ON to OFF ChAT cells was about 70 to 30 in human and 30 to 70 in marmoset. Our results show that there are species-related differences between different primates with respect to the expression of calbindin.

Morphology of human retinal ganglion cells with intraretinal axon collaterals

1998 ◽  
Vol 15 (2) ◽  
pp. 377-387 ◽  
Author(s):  
BETH B. PETERSON ◽  
DENNIS M. DACEY
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Plexiform Layer ◽  
Wide Field ◽  
Inner Plexiform Layer ◽  
Human Retina ◽  
Cell Type ◽  
Axon Collaterals

Ganglion cells with intraretinal axon collaterals have been described in monkey (Usai et al., 1991), cat (Dacey, 1985), and turtle (Gardiner & Dacey, 1988) retina. Using intracellular injection of horseradish peroxidase and Neurobiotin in in vitro whole-mount preparations of human retina, we filled over 1000 ganglion cells, 19 of which had intraretinal axon collaterals and wide-field, spiny dendritic trees stratifying in the inner half of the inner plexiform layer. The axons were smooth and thin (∼2 μm) and gave off thin (<1 μm), bouton-studded terminal collaterals that extended vertically to terminate in the outer half of the inner plexiform layer. Terminal collaterals were typically 3–300 μm in length, though sometimes as long as 700 μm, and were present in clusters, or as single branched or unbranched varicose processes with round or somewhat flattened lobular terminal boutons 1–2 μm in diameter. Some cells had a single axon whereas other cells had a primary axon that gave rise to 2–4 axon branches. Axons were located either in the optic fiber layer or just beneath it in the ganglion cell layer, or near the border of the ganglion cell layer and the inner plexiform layer. This study shows that in the human retina, intraretinal axon collaterals are associated with a morphologically distinct ganglion cell type. The synaptic connections and functional role of these cells are not yet known. Since distinct ganglion cell types with intraretinal axon collaterals have also been found in monkey, cat, and turtle, this cell type may be common to all vertebrate retinas.

Nicotinic acetylcholine receptors in the ground squirrel retina: Localization of the β4 subunit by immunohistochemistry and in situ hybridization

1994 ◽  
Vol 11 (3) ◽  
pp. 569-577 ◽  
Author(s):  
Luiz R. G. Britto ◽  
Scott W. Rogers ◽  
Dânia E. Hamassaki-Britto ◽  
Robert M. Duvoisin
Keyword(s):  
Ganglion Cell ◽  
Nicotinic Acetylcholine Receptors ◽  
Ground Squirrel ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Inner Nuclear Layer ◽  
Nachr Subunit

AbstractImmunohistochemical and in situ hybridization techniques were used to localize the β4 subunit of the neuronal nicotinic acetylcholine receptors (nAChRs) in the ground squirrel retina. The β4 nAChR subunit was detected in both transverse and horizontal sections of the retina using a subunit-specific antiserum and the avidin-biotin complex technique. Two bands of labeled processes were seen in the inner plexiform layer, corresponding approximately to the laminae where the cholinergic cells arborize. Labeled cells were found in the ganglion cell layer and the inner third of the inner nuclear layer. The cells in the ganglion cell layer were medium- to large-sized and were frequently observed to give rise to axon-like processes. Most of the labeled neurons in the inner nuclear layer were small presumptive amacrine cells, but a few medium-to-large cells were also labeled. These could constitute a different class of amacrine cells or displaced ganglion cells. The latter possibility is supported by the existence of nAChR-containing displaced ganglion cells in the avian retina. In situ hybridization with a 35S-labeled cRNA probe revealed the expression of mRNA coding for the nAChR β4 subunit in the ganglion cell layer and the inner third of the inner nuclear layer. This finding confirmed the immunohistochemical data of the cellular localization of β4 nAChR subunit.These results indicate that the β4 nAChR subunit is expressed by specific subtypes of neurons on the ground squirrel retina. As the expression of that particular nAChR subunit appears to be very limited in the brain, the present data suggest that the retina might represent a useful model to study the function of nAChRs containing the β4 subunit.

The number, morphology, and distribution of retinal ganglion cells and optic axons in the Australian lungfishNeoceratodus forsteri(Krefft 1870)

2006 ◽  
Vol 23 (2) ◽  
pp. 257-273 ◽  
Author(s):  
HELENA J. BAILES ◽  
ANN E.O. TREZISE ◽  
SHAUN P. COLLIN
Keyword(s):  
Optic Nerve ◽  
Ganglion Cell ◽  
Retinal Ganglion Cells ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Resolving Power ◽  
Retinal Ganglion ◽  
Retrograde Labelling

Australian lungfishNeoceratodus forsterimay be the closest living relative to the first tetrapods and yet little is known about their retinal ganglion cells. This study reveals that lungfish possess a heterogeneous population of ganglion cells distributed in a horizontal streak across the retinal meridian, which is formed early in development and maintained through to adult stages. The number and complement of both ganglion cells and a population of putative amacrine cells within the ganglion cell layer are examined using retrograde labelling from the optic nerve and transmission electron-microscopic analysis of axons within the optic nerve. At least four types of retinal ganglion cells are present and lie predominantly within a thin ganglion cell layer, although two subpopulations are identified, one within the inner plexiform and the other within the inner nuclear layer. A subpopulation of retinal ganglion cells comprising up to 7% of the total population are significantly larger (>400 μm2) and are characterized as giant or alpha-like cells. Up to 44% of cells within the retinal ganglion cell layer represent a population of presumed amacrine cells. The optic nerve is heavily fasciculated and the proportion of myelinated axons increases with body length from 17% in subadults to 74% in adults. Spatial resolving power, based on ganglion cell spacing, is low (1.6–1.9 cycles deg−1,n= 2) and does not significantly increase with growth. This represents the first detailed study of retinal ganglion cells in sarcopterygian fish, and reveals that, despite variation amongst animal groups, trends in ganglion cell density distribution and characteristics of cell types were defined early in vertebrate evolution.

Most calretinin-containing amacrine cells in the rabbit retina co-localize glycine

1999 ◽  
Vol 16 (6) ◽  
pp. 983-990 ◽  
Author(s):  
ROBERT GÁBRIEL ◽  
BÉLA VÖLGYI ◽  
EDIT POLLÁK
Keyword(s):  
Ganglion Cell ◽  
Calcium Binding ◽  
Binding Proteins ◽  
Ganglion Cell Layer ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Small Population ◽  
Calcium Binding Proteins ◽  
Rabbit Retina ◽  
Fiber Layer

Calretinin-containing retinal amacrine cells are heterogeneous with regard to their neurochemical properties. In the rabbit retina, about 90% of them contain glycine, as evidenced in the present study by double-label immunocytochemistry. In a previous report, we showed that a small population of amacrine cells contains both γ-aminobutyric acid and calretinin. In this study, we further identified this cell population by means of known secondary markers. However, none of the markers we tested (choline acetyltransferase, serotonin accumulation, NADPH-diaphorase, vasoactive intestinal polypeptide) co-localized with calretinin. A small population (1%) of the cells in the ganglion cell layer contains both calretinin and glycine. Since calretinin-positive cells in the ganglion cell layer have been identified as ganglion cells based on soma size and presence of calretinin-positive axons in the optic nerve fiber layer, this population may represent a class of ganglion cell which contains glycine. Our results, together with those of other studies, suggest that calretinin is not a general marker of any of the well-known amacrine cell types in the mammalian retina. Rather, calretinin, just as other calcium-binding proteins, is distributed in a species-specific manner. At the same time it appears that, as shown for horizontal cells, one or more of the major buffer-type calcium-binding proteins of the EF-hand family is present in most of the retinal amacrine cells.

Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta)

1989 ◽  
Vol 2 (4) ◽  
pp. 331-338 ◽  
Author(s):  
William D. Eldred ◽  
Kristin Cheung
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Rabbit Antiserum ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Outer Plexiform Layer ◽  
Inner Plexiform Layer ◽  
Synaptic Interactions

AbstractWe have localized glycine-like immunoreactivity to provide new anatomical detail about glycinergic neurons in the turtle retina. A rabbit antiserum directed against a glycine/albumin conjugate was used with standard fluorescent and avidin-biotin labeling techniques. Some processes in the outer plexiform layer and many processes in the inner plexiform layer, numerous somata in the inner nuclear layer, and isolated somata in the ganglion cell layer were immunoreactive.The vast majority of labeled neurons were amacrine cells. One class of amacrine cells had well-labeled somata near the inner nuclear/inner plexiform layer border, which gave rise to thick primary processes that entered the inner plexiform layer and arborized near the border of strata 1 and 2 and in stratum 3. A second class of glycinergic neurons, consisting of putative interplexiform cells, was unique in that it gave rise to dendritic arborizations in both the outer plexiform layer and the inner plexiform layer. Some of the immunoreactive neurons in the ganglion cell layer were apparently displaced amacrine cells, while others were probably true ganglion cells because they gave rise to labeled axons, and many labeled axons were visible in the ganglion cell axon layer. These results suggested that glycine played an extensive role in the turtle retina, and that it was involved in many diverse synaptic interactions in both the outer plexiform layer and the inner plexiform layer.

Development of the rabbit retina, III: Differential retinal growth, and density of projection neurons and interneurons

1993 ◽  
Vol 10 (3) ◽  
pp. 479-498 ◽  
Author(s):  
A. Reichenbach ◽  
J. Schnitzer ◽  
E. Reichelt ◽  
N. N. Osborne ◽  
B. Fritzsche ◽  
...  
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Quantitative Description ◽  
Müller Cells ◽  
Amacrine Cells ◽  
Projection Neurons ◽  
Muller Cells ◽  
Single Plane

AbstractTo provide a quantitative description of postnatal retinal expansion in rabbits, a new procedure was developed to map the retinae, which cover the inner surface of hemispheres or parts of rotation ellipsoids, in situ, onto a single plane. This method, as well as the known distribution of Müller cells per unit retinal surface area, were used to estimate the redistribution of specific subpopulations of Müller cells within different topographic regions of the retinae. Müller cells are known to exist as a stable population of cells 1 week after birth and can therefore be used as “markers” for determining tissue expansion. Our results show that differential retinal expansion occurs during development. Peripheral retinal regions expand at least twice as much as the central ones. Furthermore, there is a greater vertical than horizontal expansion. This differential retinal expansion leads to a corresponding redistribution of 5-hydroxytryptamine (5-HT) accumulating amacrine cells. Differential retinal expansion, however, does not account for all of the changes in the centro-peripheral density gradient of cells in the ganglion cell layer (GCL) — mostly retinal ganglion cells — during postnatal development. The changes in the ganglion cell layer were evaluated in Nissl-stained wholemount retinal preparations. Additionally, the difference between expansion-related redistribution of cells in the GCL and Müller cells was confirmed in wholemount preparations where Müller cells (identified as vimentin positive) and cells in the GCL (identified by fluorescent supravital dyes) were simultaneously labeled. It is assumed that many of the ganglion cells within the retinal center are not translocated during retinal expansion, possibly because their axons are fixed. In contrast, 5-HT accumulating amacrine cells — which are interneurons without a retinofugal axon — display a passive redistribution together with the surrounding retinal tissue.

Microtubule-associated protein 1A (MAP 1A) is a ganglion cell marker in adult rat retina

1989 ◽  
Vol 2 (4) ◽  
pp. 349-356 ◽  
Author(s):  
Lisa McKerracher ◽  
Richard B. Vallee ◽  
Albert J. Aguayo
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Inner Plexiform Layer ◽  
Double Labeling ◽  
Rat Retina ◽  
Adult Rat ◽  
Cell Somata

AbstractWe have used antibodies raised against a cytoskeletal protein, microtubule-associated protein 1A (MAP 1A), to stain adult rat retina. In cryostat and polyethylene glycol-embedded radial sections, the fiber layer, ganglion cell layer, and inner plexiform layer were highly immunoreactive, a finding that suggested that the ganglion cell somata, axons, and dendrites were recognized by these antibodies. Retrograde labeling of retinal cell somata from the superior colliculus and dorso-lateral geniculate nucleus to identify ganglion cells showed colocalization of the tracer and immunoreactive cells. Double labeling with nuclear stains revealed that many cells in the ganglion cell layer, which are likely displaced amacrine cells, were not recognized by these antibodies. Furthermore, transection of ganglion cell axons, a procedure that causes retrograde degeneration of many of the axotomized ganglion cells, led to a decrease in the number of anti-MAP 1A immunoreactive cells in retinal wholemounts. Thus, MAP 1A antibodies preferentially stain ganglion cell somata and dendrites but not amacrine cells. These antibodies should be useful ganglion cell markers.

The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system

1994 ◽  
Vol 11 (2) ◽  
pp. 401-409 ◽  
Author(s):  
Debora L. Nickla ◽  
Michael D. Gottlieb ◽  
Gonzalo Marin ◽  
Ximena Rojas ◽  
Luiz R. G. Britto ◽  
...  
Keyword(s):  
Ganglion Cell ◽  
Cytochrome Oxidase ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Target Cells ◽  
Inner Plexiform Layer ◽  
Optic System ◽  
Accessory Optic System

AbstractIn birds, neurons of the isthmo-optic nucleus (ION), as well as “ectopic” neurons, send axons to the retina, where they synapse on cells in the inner nuclear layer (INL). Previous work has shown that centrifugal axons can be divided into two anatomically distinct types depending on their mode of termination: either “convergent” or “divergent” (Ramon y Cajal, 1889; Maturana & Frenk, 1965). We show that cytochrome-oxidase histochemistry specifically labels “convergent” centrifugal axons and target neurons which appear to be amacrine cells, as well as three “types” of ganglion cells: two types found in the INL (displaced ganglion cells) and one in the ganglion cell layer. Labeled target amacrine cells have distinct darkly labeled “nests” of boutons enveloping the somas, are associated with labeled centrifugal fibers, and are confined to central retina. Lesions of the isthmo-optic tract abolish the cytochrome-oxidase labeling in the centrifugal axons and in the target amacrine cells but not in the ganglion cells. Cytochrome-oxidase-labeled ganglion cells in the INL are large; one type is oval and similar to the classical displaced ganglion cells of Dogiel, which have been reported to receive centrifugal input; the other type is rounder. Rhodamine beads injected into the accessory optic system results in retrograde label in both types of cells, showing that two distinct types of displaced ganglion cells project to the accessory optic system in chickens. The ganglion cells in the ganglion cell layer that label for cytochrome oxidase also project to the accessory optic system. These have proximal dendrites that ramify in the outer inner plexiform layer. Neither the target amacrine cells nor either of the displaced ganglion cells are immunoreactive for the inhibitory transmitter gamma aminobutyric acid. At least some of the target amacrine cells may, however, be cholinoceptive: we found that the antibody to the alpha-7 subunit of the nicotinic ACh receptor labels a population of cells in the INL that are similar in location, size, and the presence of labeled bouton-like structures to those we find labeled with cytochrome oxidase. This antibody also labels neurons in the ION proper but not ectopic cells. In conclusion, it appears that cytochrome oxidase may be a marker for “convergent” centrifugal axons and at least one of their target cells in the INL.

Displaced GAD65 amacrine cells of the guinea pig retina are morphologically diverse

2006 ◽  
Vol 23 (6) ◽  
pp. 931-939 ◽  
Author(s):  
YEN-HONG KAO ◽  
PETER STERLING
Keyword(s):  
Guinea Pig ◽  
Ganglion Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Cell Types ◽  
The Other ◽  
Mammalian Retina ◽  
Visual Streak

The ganglion cell layer of mammalian retina contains numerous amacrine cells. Many belong to one type, the cholinergic starburst cell, but the other types have not been systematically identified. Using a new method to target sparsely represented cell types, we filled about 200 amacrine neurons in the ganglion cell layer of the guinea pig visual streak and identified 11 types. Ten of these resemble types identified in other species with somas in the inner nuclear layer, but one type has not been previously reported. Most of the types and nearly all the injected cells (95%) arborized low in the synaptic layer where they would co-stratify with various classes of ON ganglion cell. The displaced somas (7% of all amacrine cells) thus represent a heterogeneous pool, which are relatively accessible for study of their interactions with ON ganglion cells.

scholarly journals HCN4-like immunoreactivity in rat retinal ganglion cells

2008 ◽  
Vol 25 (1) ◽  
pp. 95-102 ◽  
Author(s):  
HANAKO OI ◽  
GLORIA J. PARTIDA ◽  
SHERWIN C. LEE ◽  
ANDREW T. ISHIDA
Keyword(s):  
Ganglion Cell ◽  
Retinal Ganglion Cells ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Mouse Retina ◽  
Intracellular Camp ◽  
Retinal Ganglion ◽  
Hcn Channel

Antisera directed against hyperpolarization-activated, cyclic nucleotide–sensitive (HCN) channels bind to somata in the ganglion cell layer of rat and rabbit retinas, and mRNA for different HCN channel isoforms has been detected in the ganglion cell layer of mouse retina. However, previous studies neither provided evidence that any of the somata are ganglion cells (as opposed to displaced amacrine cells) nor quantified these cells. We therefore tested whether isoform-specific anti-HCN channel antisera bind to ganglion cells labeled by retrograde transport of fluorophore-coupled dextran. In flat-mounted adult rat retinas, the number of dextran-backfilled ganglion cells agreed with cell densities reported in previous studies, and anti-HCN4 antisera bound to the somata of approximately 40% of these cells. The diameter of these somata ranged from 7 to 30 μm. Consistent with localization to cell membranes, the immunoreactivity formed a thin line that circumscribed individual somata. Optic fiber layer axon fascicles, and the proximal dendrites of some ganglion cells, also displayed binding of anti-HCN4 antisera. These results suggest that the response of some mammalian retinal ganglion cells to hyperpolarization may be modulated by changes in intracellular cAMP levels, and could thus be more complex than expected from previous voltage and current recordings.

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