Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immunocytochemical study

1994 ◽  
Vol 11 (6) ◽  
pp. 1115-1134 ◽  
Author(s):  
D.V. Pow ◽  
O.K. Crook ◽  
R.O.L. Wong

AbstractWe have studied, by immunocytochemistry, the ontogeny of GABA, glycine, glutamate, glutamine, and taurine-containing cells in the rabbit retina. Amacrine cells show GABA immunoreactivity by embryonic day 25 (E25) and throughout postnatal life. By contrast, ganglion cells and horizontal cells are only transiently GABA-immunoreactive (-IR); few appear GABA-IR by the third postnatal week. At maturity, glycine is present in amacrine cells and in some bipolar cells. During development, putative ganglion cells transiently contained glycine between E25 and postnatal day 3 (P3), whereas immunolabelling in presumed amacrine cells and bipolar cells persists after birth. Ganglion cells, bipolar cells, photoreceptors, and some amacrine cells are glutamate-IR in the adult retina. Glutamate immunoreactivity first appears in the somata and processes of cytoblastic cells by E20 and is prominent by E25. Surprisingly, ganglion cells are not strongly glutamate-IR until just before eye-opening, at postnatal day 10 (P10), coincident with the appearance of glutamine in their somata and in Müller glial cells. Bipolar cells are glutamate-IR before they or Müller cells contain high levels of glutamine (at P10). Glutamate immunoreactivity in photoreceptors is progressively restricted to the inner segments by eye-opening. At no stage are presumed horizontal cells glutamate-IR or glutamine-IR, but some amacrine cells show glutamate- and glutamine-IR by P10. Taurine is localized to photoreceptors and Müller glial in the adult retina. Some cytoblasts are taurine-IR at E20; with ensuing development, taurine labelling becomes restricted primarily to Müller cells and photoreceptors; some putative bipolar cells may also be labelled. However, for a few days around birth, cells resembling horizontal cells, also show taurine immunoreactivity. The early appearance and often transient expression of these amino acids in retinal cells suggests that these neuroactive molecules may be involved in the structural and functional development of the retina.

1992 ◽  
Vol 9 (3-4) ◽  
pp. 313-323 ◽  
Author(s):  
David M. Sherry ◽  
Robert J. Ulshafer

AbstractImmunocytochemical and autoradiographic methods were used to identify neurons in the pure cone retina of the lizard (Anolis carolinensis) that are likely to employ glutamate (GLU) or aspartate (ASP) as a neurotransmitter.GLU immunocytochemistry demonstrated high levels of endogenous GLU in all cone types and numerous bipolar cells. Moderate GLU levels were found in horizontal and ganglion cells. Müller cells and most amacrine cells had very low GLU levels. GLU immunoreactivity (GLU-IR) in the cones was present from the inner segment to the synaptic pedicle. A large spherical cell type with moderate GLU-IR was identified in the proximal inner plexiform layer (IPL). These cells also contain ASP and have been tentatively identified as amacrine cells. Uptake of [3H]-L-GLU labeled all retinal layers. All cone types and Müller cells sequestered [3H]-D-ASP, a substrate specific for the GLU transporter.Anti-ASP labeling was observed in cones, horizontal cells, amacrine cells, and cells in the ganglion cell layer. ASP immunoreactivity (ASP-IR) in the cones was confined to the inner segment. One ASP-containing pyriform amacrine cell subtype ramifying in IPL sublamina b was identified.Analysis of GLU-IR, ASP-IR, and GABA-IR on serial sections indicated that there were two distinct populations of horizontal cells in the Anolis retina: one containing GABA-IR, GLU-IR, and ASP-IR; and another type containing only GLU-IR and ASP-IR. Light GLU-IR was frequently found in GABA-containing amacrine cells but ASP-IR was not.The distinct distributions of GLU and ASP may indicate distinctly different roles for these amino acids. GLU, not ASP, is probably the major neurotransmitter in the cone-biploar-ganglion cell pathway of the Anolis retina. Both GLU and ASP are present in horizontal cells and specific subpopulations of amacrine cells, but it is unclear if GLU or ASP have a neurotransmitter role in these cells.


1994 ◽  
Vol 11 (6) ◽  
pp. 1193-1203 ◽  
Author(s):  
Chen-Yu Yang ◽  
Stephen Yazulla

AbstractThe presence of inhibitory bipolar cells in salamander retina was investigated by a comparative analysis of the distribution of glutamate- and GABA-immunoreactivities (GLU-IR; GABA-IR) using a postembedding immunocytochemical method. GLU-IR was found in virtually all photoreceptors, bipolar cells and ganglion cells, neuronal elements that transfer information vertically through the retina. GLU-IR also was found in numerous amacrine cells in the mid and proximal inner nuclear layer as well as in the cytoplasm of horizontal cells, while the nucleus of horizontal cells was either lightly labeled or not labeled at all. GLU-IR was found in the outer plexiform layer and intensely in the inner plexiform layer, in which there was no apparent sublamination. Forty-seven percent of Type IB bipolar cells in the distal inner nuclear layer and 13% of the displaced bipolar cells were GABA-IR. All bipolar cells were also GLU-IR, indicating that GABA-IR bipolar cells were a subset of GLU-IR bipolar cells rather than a separate population. About 12% of the Type IB bipolar cells were moderately GABA-IR and likely comprised a GABAergic subtype. GLU-IR levels in the presumed GABAergic bipolar cells were higher than in other purely GLU-IR bipolar cells suggesting that these GABA-IR bipolar cells are glutamatergic as well. All of the displaced bipolar cells were only lightly GABA-IR, indicating that displaced bipolar cells comprise a more homogeneous class of glutamatergic cell than orthotopic bipolar cells. GAD-IR co-localized with GABA-IR in orthotopic but not displaced bipolar cells, further supporting the idea that some orthotopic bipolar cells are GABAergic. A small proportion of bipolar cells in salamander retina contain relatively high levels of both GABA and glutamate. Co-release of these substances by bipolar cells could contribute to the “push-pull” modulation of ganglion cell responses.


1975 ◽  
Vol 38 (1) ◽  
pp. 53-71 ◽  
Author(s):  
K. Naka ◽  
N. R. Garraway

The morphology of the catfish horizontal cells is comparable to that in other fish retinas. The external horizontal cells contact cone receptors and are stellate in shape; the intermediate horizontal cells are even more so and contact rod receptors. The internal horizontal cells constitute the most proximal layer of the inner nuclear layer and may possibly be, in reality, extended processes from the other two horizontal cell types. Bipolar cells resemble those in other teleost retinas: the size and shape of their dendritic tree encompass a continuous spectrum ranging from what is known as the small to the large bipolar cells. The accepted definition of amacrine cells is sufficiently vague to justify our originating a more descriptive and less inferential name for the (axonless) neurons in the inner nuclear layer which radiate processes throughout the inner synaptic layer. These starbust and spaghetti cells vary considerably in the character and extent of their dendritic spread, but correlates exist in other vertebrate retinas. Ganglion cells are found not only in the classical ganglion layer but displaced into the inner nuclear layer as well. Several types can be distinguished on the basis of cell geometry and by the properties of their dendritic tree. Not all of the categorization corresponds with previous descriptions; our findings suggest that some reorganization may be necessary in the accepted classification of cells in the proximal areas of the vertebrate retina. A subtle yet remarkable pattern underlies the entire structure of the catfish retina; there exists a definite gradient of size within a particular class of cells, and of configuration among the subclasses of a specific cell type. It remains to be seen if these morphological spectra bear any functional consequences. The fact that the structure of the catfish retina most closely resembles those of other phylogenetically ancient animals, such as the skate and the dogfish shark, testifies to its primitive organization; morphological and functional mechanisms discernible in this simple system may, therefore, be applicable to the retinas of higher ordered vertebrates.


2019 ◽  
Vol 36 ◽  
Author(s):  
Andrea S. Bordt ◽  
Diego Perez ◽  
Luke Tseng ◽  
Weiley Sunny Liu ◽  
Jay Neitz ◽  
...  

AbstractThere are more than 30 distinct types of mammalian retinal ganglion cells, each sensitive to different features of the visual environment. In rabbit retina, they can be grouped into four classes according to their morphology and stratification of their dendrites in the inner plexiform layer (IPL). The goal of this study was to describe the synaptic inputs to one type of Class IV ganglion cell, the third member of the sparsely branched Class IV cells (SB3). One cell of this type was partially reconstructed in a retinal connectome developed using automated transmission electron microscopy (ATEM). It had slender, relatively straight dendrites that ramify in the sublamina a of the IPL. The dendrites of the SB3 cell were always postsynaptic in the IPL, supporting its identity as a ganglion cell. It received 29% of its input from bipolar cells, a value in the middle of the range for rabbit retinal ganglion cells studied previously. The SB3 cell typically received only one synapse per bipolar cell from multiple types of presumed OFF bipolar cells; reciprocal synapses from amacrine cells at the dyad synapses were infrequent. In a few instances, the bipolar cells presynaptic to the SB3 ganglion cell also provided input to an amacrine cell presynaptic to the ganglion cell. There was apparently no crossover inhibition from narrow-field ON amacrine cells. Most of the amacrine cell inputs were from axons and dendrites of GABAergic amacrine cells, likely providing inhibitory input from outside the classical receptive field.


2005 ◽  
Vol 22 (4) ◽  
pp. 535-549 ◽  
Author(s):  
JIAN ZHANG ◽  
WEI LI ◽  
HIDEO HOSHI ◽  
STEPHEN L. MILLS ◽  
STEPHEN C. MASSEY

The correlation between cholinergic sensitivity and the level of stratification for ganglion cells was examined in the rabbit retina. As examples, we have used ON or OFF α ganglion cells and ON/OFF directionally selective (DS) ganglion cells. Nicotine, a cholinergic agonist, depolarized ON/OFF DS ganglion cells and greatly enhanced their firing rates but it had modest excitatory effects on ON or OFF α ganglion cells. As previously reported, we conclude that DS ganglion cells are the most sensitive to cholinergic drugs. Confocal imaging showed that ON/OFF DS ganglion cells ramify precisely at the level of the cholinergic amacrine cell dendrites, and co-fasciculate with the cholinergic matrix of starburst amacrine cells. However, neither ON or OFF α ganglion cells have more than a chance association with the cholinergic matrix. Z-axis reconstruction showed that OFF α ganglion cells stratify just below the cholinergic band in sublamina a while ON α ganglion cells stratify just below cholinergic b. The latter is at the same level as the terminals of calbindin bipolar cells. Thus, the calbindin bipolar cell appears to be a prime candidate to provide the bipolar cell input to ON α ganglion cells in the rabbit retina. We conclude that the precise level of stratification is correlated with the strength of cholinergic input. Alpha ganglion cells receive a weak cholinergic input and they are narrowly stratified just below the cholinergic bands.


2013 ◽  
Vol 30 (3) ◽  
pp. 91-103 ◽  
Author(s):  
MERVE TEKMEN-CLARK ◽  
EVANNA GLEASON

AbstractNitric oxide (NO) is known to exert multiple effects on the function of many retinal neurons and their synapses. Therefore, it is equally important to understand the potential sources of NO within the retina. To explore this, we employ a combination of 4-amino-5-methylamino-2′,7′-difluorofluorescein diacetate (DAF-FM) based NO detection and immunohistochemistry for the NO synthetic enzymes, neuronal and endothelial nitric oxide synthase (nNOS and eNOS). We find DAF signals in photoreceptors, horizontal cells, amacrine cells, efferent synapses, Müller cells, and cells in the ganglion cell layer (GCL). nNOS immunoreactivity was consistent with the DAF signal with the exception that horizontal cells and Müller cells were not clearly labeled. eNOS-like immunoreactivity (eNOS-LI) was more widespread with photoreceptors, horizontal cells, occasional bipolar cells, amacrine cells, Müller cells, and cells in the GCL all showing labeling. Double labeling with antibodies raised against calretinin, syntaxin, and glutamine synthetase confirmed that horizontal cells, amacrine cells, and Müller cells (respectively) were expressing eNOS-LI. Although little or no nNOS labeling is observed in horizontal cells or Müller cells, the expression of eNOS-LI is consistent with the ability of these cells to produce NO. Together these results suggest that the capability to produce NO is widespread in the chicken retina. We propose that multiple forms of regulation for nNOS and eNOS play a role in the patterning of NO production in the chicken retina.


2000 ◽  
Vol 17 (1) ◽  
pp. 1-9 ◽  
Author(s):  
DAVID V. POW ◽  
ANITA E. HENDRICKSON

Previous studies show that glycine transporter-1 (glyt-1) is a consistent membrane marker of adult retinal neurons that are likely to release glycine at their synaptic terminals (Pow, 1998; Vaney et al., 1998; Pow & Hendrickson, 1999). The current study investigated when glyt-1 immunoreactivity appeared in the postnatal rat retina, and whether all glycine-containing neurons also labelled for glyt-1. Ganglion cells, horizontal cells, and photoreceptors showed transient labelling. Many cells in the ganglion cell layer are immunoreactive for both glycine and glyt-1 at postnatal day (Pd) 1 but both are minimal by Pd5. Transient immunoreactivity for both glyt-1 and glycine was observed in presumptive horizontal cells between Pd5 and Pd10. At Pd1 many cells in the outer part of the retina which resembled immature photoreceptors were heavily labelled for glycine, but did not express glyt-1; these disappeared at older ages. These findings suggest diverse mechanisms and transient roles for glycine in the developing rat retina. In the adult rat retina, a subpopulation of amacrine cells are prominently immunoreactive for both glycine and glyt-1. These cells labelled for glycine at Pd1, but did not express significant levels of glyt-1 until Pd5. Processes from these amacrine cells did not reach the inner half of the inner plexiform layer until Pd10–14. Bipolar cells became glycine-IR between Pd10 and Pd14, but consistently lacked any glyt-1 immunoreactivity. This temporal pattern of labelling strongly indicates that bipolar cells label for glycine when gap junctions become functional between glycine/glyt-1 immunoreactive amacrine cells and cone bipolar cells.


1998 ◽  
Vol 80 (1) ◽  
pp. 447-451 ◽  
Author(s):  
Adam L. Jacobs ◽  
Frank S. Werblin

Jacobs, Adam L. and Frank S. Werblin. Spatiotemporal patterns at the retinal output. J. Neurophysiol. 80: 447–451, 1998. Edge enhancement in the retina is thought to be mediated by classical center-surround antagonism, first encountered as the interactions between horizontal cells and cones. But in the salamander retina these interactions do little to enhance edges. Instead, a robust dynamic interaction between amacrine and bipolar cells appears to be responsible for a sharp edge enhancement. To demonstrate this we recorded extracellularly from a single ganglion cell and moved a flashed square, 300 μm on a side, over a 1.5 × 1.0 mm2 grid at 25-μm increments. Playing back all of these recordings simultaneously simulated the pattern of responses that would have been measured from an array of ganglion cells. The emerging pattern of ganglion cell activity first faithfully represented the flashed square, but after ∼60 ms the center of the representation collapsed, leaving a representation of only the edges. We inferred that the feedback synapse from amacrine to bipolar cells at γ-aminobutyric acid-C (GABAC) receptors mediated this effect: bicuculline and strychnine were ineffective in altering the response pattern, but in picrotoxin the center of the representation did not collapse. The GABAergic amacrine cells thought to mediate this effect have quite narrow spread of processes, so the existence of this edge-enhancing effect suggests a mechanism quite different from classical lateral inhibition, namely the delayed inhibition of a spatially expanding input pattern.


2009 ◽  
Vol 364 (1531) ◽  
pp. 2911-2924 ◽  
Author(s):  
Trevor D. Lamb

Recent findings shed light on the steps underlying the evolution of vertebrate photoreceptors and retina. Vertebrate ciliary photoreceptors are not as wholly distinct from invertebrate rhabdomeric photoreceptors as is sometimes thought. Recent information on the phylogenies of ciliary and rhabdomeric opsins has helped in constructing the likely routes followed during evolution. Clues to the factors that led the early vertebrate retina to become invaginated can be obtained by combining recent knowledge about the origin of the pathway for dark re-isomerization of retinoids with knowledge of the inability of ciliary opsins to undergo photoreversal, along with consideration of the constraints imposed under the very low light levels in the deep ocean. Investigation of the origin of cell classes in the vertebrate retina provides support for the notion that cones, rods and bipolar cells all originated from a primordial ciliary photoreceptor, whereas ganglion cells, amacrine cells and horizontal cells all originated from rhabdomeric photoreceptors. Knowledge of the molecular differences between cones and rods, together with knowledge of the scotopic signalling pathway, provides an understanding of the evolution of rods and of the rods' retinal circuitry. Accordingly, it has been possible to propose a plausible scenario for the sequence of evolutionary steps that led to the emergence of vertebrate photoreceptors and retina.


1999 ◽  
Vol 16 (6) ◽  
pp. 1105-1114 ◽  
Author(s):  
PU QIN ◽  
ROBERTA G. POURCHO

AMPA-selective glutamate receptors play a major role in glutamatergic neurotransmission in the retina and are expressed in a variety of neuronal subpopulations. In the present study, immunocytochemical techniques were used to visualize the distribution of GluR2 and GluR4 subunits in the cat retina. Results were compared with previous localizations of GluR1 and GluR2/3. Staining for GluR2 was limited to a small number of amacrine and ganglion cells whereas GluR4 staining was present in A-type horizontal cells, many amacrine cells including type AII amacrine cells, and the majority of the cells in the ganglion cell layer. Analysis of synaptic relationships in the outer plexiform layer showed the GluR4 subunit to be concentrated at the contacts of cone photoreceptors with A-horizontal cells. In the inner plexiform layer, both GluR2 and GluR4 were postsynaptic to cone bipolar cells at dyad contacts although GluR2 staining was limited to one of the postsynaptic elements whereas GluR4 immunoreactivity was often seen in both postsynaptic elements. Unlike GluR2, GluR4 was also postsynaptic to rod bipolar cells where it could be visualized in processes of AII amacrine cells. The data indicate that GluR3 and GluR4 subunits are colocalized in a number of cell types including A-type horizontal cells, AII amacrine cells, and alpha ganglion cells, but whether they are combined in the same multimeric receptors remains to be determined.


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