Midget and parasol ganglion cells of the primate retina express the α1 subunit of the glycine receptor

1999 ◽  
Vol 16 (5) ◽  
pp. 957-966 ◽  
Author(s):  
ULRIKE GRÜNERT ◽  
KRISHNA K. GHOSH

Glycine is a major inhibitory neurotransmitter in the mammalian retina and has been shown to influence the responses of ganglion cells. Midget and parasol ganglion cells serve distinct physiological roles in the primate retina and show differences in their response characteristics to light stimuli. In the present study, we addressed the question of whether the expression of glycine receptors differs in midget and parasol ganglion cells. Ganglion cells in the retinae of marmoset and macaque monkeys were injected with Neurobiotin in a live in vitro retinal whole-mount preparation. Retinal pieces were then processed with an antibody against the α1 subunit of the glycine receptor. Strong punctate immunoreactivity indicative of synaptic localization is present in the ON and OFF sublamina of the inner plexiform layer. Many of the immunoreactive puncta coincide with the dendrites of both midget and parasol ganglion cells. Immunoreactive puncta are present on distal and proximal dendrites of ON and OFF cells. These results suggest that ON and OFF midget and parasol cells do not differ with respect to the distribution of the α1 subunit of the glycine receptor.

1992 ◽  
Vol 9 (3-4) ◽  
pp. 279-290 ◽  
Author(s):  
Dennis M. Dacey ◽  
Sarah Brace

AbstractIntracellular injections of Neurobiotin were used to determine whether the major ganglion cell classes of the macaque monkey retina, the magnocellular-projecting parasol, and the parvocellular-projecting midget cells showed evidence of cellular coupling similar to that recently described for cat retinal ganglion cells. Ganglion cells were labeled with the fluorescent dye acridine orange in an in vitro, isolated retina preparation and were selectively targeted for intracellular injection under direct microscopic control. The macaque midget cells, like the beta cells of the cat's retina, showed no evidence of tracer coupling when injected with Neurobiotin. By contrast, Neurobiotin-filled parasol cells, like cat alpha cells, showed a distinct pattern of tracer coupling to each other (homotypic coupling) and to amacrine cells (heterotypic coupling).In instances of homotypic coupling, the injected parasol cell was surrounded by a regular array of 3–6 neighboring parasol cells. The somata and proximal dendrites of these tracer-coupled cells were lightly labeled and appeared to costratify with the injected cell. Analysis of the nearest-neighbor distances for the parasol cell clusters showed that dendritic-field overlap remained constant as dendritic-field size increased from 100–400 μm in diameter.At least two amacrine cell types showed tracer coupling to parasol cells. One amacrine type had a small soma and thin, sparsely branching dendrites that extended for 1–2 mm in the inner plexiform layer. A second amacrine type had a relatively large soma, thick main dendrites, and distinct, axon-like processes that extended for at least 2–3 mm in the inner plexiform layer. The main dendrites of the large amacrine cells were closely apposed to the dendrites of parasol cells and may be the site of Neurobiotin transfer between the two cell types. We suggest that the tracer coupling between neighboring parasol cells takes place indirectly via the dendrites of the large amacrine cells and provides a mechanism, absent in midget cells, for increasing parasol cell receptive-field size and luminance contrast sensitivity.


Development ◽  
1975 ◽  
Vol 33 (4) ◽  
pp. 915-940
Author(s):  
S. H. Chung ◽  
R. Victoria Stirling ◽  
R. M. Gaze

The structural transformations of the larval Xenopus retina at successive stages of development, and concomitant changes in response characteristics of retinal ganglion cells, were studied using histological and electrophysiological techniques. The first sign of visually evoked electrical responses appears at about the time when the ganglion cells spread out into a single layer and shortly after the inner and outer plexiform layers become discernible. Initially giving simple ‘on’ responses, the cells progressively change their response characteristics and become ‘event’ units. Subsequently, ‘dimming’ units can be identified. Throughout larval life, response properties of these two types become more distinct from one another and approximate to those found in the adult. So do the arborization patterns of the dendritic trees of the ganglion cells. Two types of branching patterns are identifiable in Golgi preparations. Around metamorphic climax, a new type of ganglion cell appears, coinciding with the emergence of ‘sustained’ units electrophysiologically. After metamorphosis, the retina still grows both in thickness (mainly in the inner plexiform layer) and diameter. The three unit types change such that they come to show pronounced inhibitory effects from the peripheral visual field on the receptive field and each unit type acquires a distinct pattern of endogenous discharge.


1991 ◽  
Vol 7 (6) ◽  
pp. 611-618 ◽  
Author(s):  
Roberta G. Pourcho ◽  
Michael T. Owczarzak

AbstractImmunocytochemical techniques were used to localize strychnine-sensitive glycine receptors in cat retina. Light microscopy showed staining in processes ramifying throughout the inner plexiform layer and in cell bodies of both amacrine and ganglion cells. At the electron-microscopic level, receptor immunoreactivity was seen to be clustered at sites postsynaptic to amacrine cells. In contrast, bipolar cells were neither presynaptic nor postsynaptic elements at sites of glycine receptor staining. Double-label studies verified the presence of glycine immunoreactivity in amacrine terminals presynaptic to glycine receptors. These findings support a role for glycine as an inhibitory neurotransmitter in amacrine cells.


1993 ◽  
Vol 10 (5) ◽  
pp. 907-914 ◽  
Author(s):  
Charles L. Zucker ◽  
Berndt Ehinger

AbstractThe distribution of glycine receptors in the turtle retina was studied with the aid of a monoclonal antibody that detects the 93-kD protein associated with the strychnine-sensitive glycine receptor. Light microscopically, receptors were found in the inner plexiform layer and, more sparsely, in the innermost parts of the inner nuclear layer. No receptors were seen to be associated with photoreceptor cells, horizontal cells, or any other structures in the distal inner nuclear layer or outer plexiform layer. Ultrastructurally, glycine receptors were found on the inner face of postsynaptic membranes of processes from amacrine and presumed ganglion cells and always involved amacrine cell processes as the presynaptic element. Such glycine receptor immunoreactive synapses onto amacrine cell processes were distributed throughout the inner plexiform layer with a peak density near the middle. On the other hand, output synapses onto ganglion cell processes displaying immunoreactive glycine receptor sites showed a bimodal distribution in the inner plexiform layer. Glycine receptor immunoreactivity was not detected on bipolar cells, but presumed glycine-utilizing processes (i.e. those presynaptic to immunoreactive glycine receptors) were occasionally found to be postsynaptic in bipolar cell dyads. The majority of the synaptic input to the presumed glycine-utilizing amacrine cell processes was from other amacrine processes, some of which were themselves glycine utilizing. The observations suggest that glycinergic synapses in the turtle retina are, to a large extent, engaged in processing interamacrine signals.


2020 ◽  
Author(s):  
Brent K. Young ◽  
Charu Ramakrishnan ◽  
Tushar Ganjawala ◽  
Yumei Li ◽  
Sangbae Kim ◽  
...  

AbstractNeurons in the CNS are distinguished from each other by their morphology, the types of the neurotransmitter they release, their synaptic connections, and their genetic profiles. While attempting to characterize the retinal bipolar cell (BC) input to retinal ganglion cells (RGCs), we discovered a previously undescribed type of interneuron in mice and primates. This interneuron shares some morphological, physiological, and molecular features with traditional BCs, such as having dendrites that ramify in the outer plexiform layer (OPL) and axons that ramify in the inner plexiform layer (IPL) to relay visual signals from photoreceptors to inner retinal neurons. It also shares some features with amacrine cells, particularly Aii amacrine cells, such as their axonal morphology and possibly the release of the inhibitory neurotransmitter glycine, along with the expression of some amacrine cell specific markers. Thus, we unveil an unrecognized type of interneuron, which may play unique roles in vision.Significance StatementCell types are the building blocks upon which neural circuitry is based. In the retina, it is widely believed that all neuronal types have been identified. We describe a cell type, which we call the Campana cell, that does not fit into the conventional neuronal retina categories but is evolutionarily conserved. Unlike retinal bipolar cells, the Campana cell receives synaptic input from both rods and cones, has broad axonal ramifications, and may release an inhibitory neurotransmitter. Unlike retinal amacrine cells, the Campana cell receives direct photoreceptor input has bipolar-like ribbon synapses. With this discovery, we open the possibility for new forms of visual processing in the retina.


2005 ◽  
Vol 22 (4) ◽  
pp. 383-393 ◽  
Author(s):  
ELIZABETH S. YAMADA ◽  
ANDREA S. BORDT ◽  
DAVID W. MARSHAK

To describe the wide-field ganglion cells, they were injected intracellularly with Neurobiotin using an in vitro preparation of macaque retina and labeled with streptavidin-Cy3. The retinas were then labeled with antibodies to choline acetyltransferase and other markers to indicate the depth of the dendrites within the inner plexiform layer (IPL) and analyzed by confocal microscopy. There were eight different subtypes of narrowly unistratified cells that ramified in each of the 5 strata, S1–5, including narrow thorny, large sparse, large moderate, large dense, large radiate, narrow wavy, large very sparse, and fine very sparse. There were four types of broadly stratified cells with dendritic trees extending from S4 to S2. One type resembled the parvocellular giant cell and another the broad thorny type described previously in primates. Another broadly stratified cell was called multi-tufted based on its distinctive dendritic branching pattern. The fourth type had been described previously, but not named; we called it broad wavy. There was a bistratified type with its major arbor in S5, the same level as the blue cone bipolar cell; it resembled the large, bistratified cell with blue ON-yellow OFF responses described recently. Two wide-field ganglion cell types were classified as diffuse because they had dendrites throughout the IPL. One had many small branches and was named thorny diffuse. The second was named smooth diffuse because it had straighter dendrites that lacked these processes. Dendrites of the large moderate and multi-tufted cells cofasciculated with ON-starburst cell dendrites and were, therefore, candidates to be ON- and ON–OFF direction-selective ganglion cells, respectively. We concluded that there are at least 15 morphoplogical types of wide-field ganglion cells in macaque retinas.


2000 ◽  
Vol 17 (3) ◽  
pp. 437-448 ◽  
Author(s):  
JOSEPH MACRI ◽  
PAUL R. MARTIN ◽  
ULRIKE GRÜNERT

The inhibitory neurotransmitter gamma aminobutyric acid (GABA) has been shown to influence the responses of ganglion cells in the mammalian retina. Consistently, GABAA receptor subunits have been localized to different ganglion cell types. In this study, the distribution of the α1 subunit of the GABAA receptor on the dendrites of midget and parasol ganglion cells was investigated quantitatively in the retina of a New World monkey, the marmoset. Ganglion cells were injected with Neurobiotin in a live in vitro retinal whole-mount preparation. Retinal pieces were then processed with an antibody against the α1 subunit of the GABAA receptor. Strong punctate immunoreactivity indicative of synaptic localization is present in the ON and OFF sublamina of the inner plexiform layer. Many of the immunoreactive puncta coincide with the dendrites of both midget and parasol ganglion cells. Immunoreactive puncta are present on distal and proximal dendrites of ON and OFF cells of both ganglion cell types. On average, parasol cells show a slight increase in the spatial density of immunoreactive puncta with distance from the soma, whereas the density of immunoreactive puncta on midget cells stays even. Parasol ganglion cells show a slightly higher average density of immunoreactive puncta (0.083 puncta/μm dendrite) than midget cells (0.054 puncta/μm dendrite).


1994 ◽  
Vol 11 (4) ◽  
pp. 721-729 ◽  
Author(s):  
U. Greferath ◽  
J. H. Brandstätter ◽  
H. Wässle ◽  
J. Kirsch ◽  
J. Kuhse ◽  
...  

AbstractImmunohistochemistry and in situ hybridization were used to study the distribution of glycine receptor (GlyR) subunits and the GlyR-associated protein gephyrin in the rat retina. Monoclonal antibodies against the α and β subunits of the GlyR and gephyrin showed a strong punctate labeling pattern in the inner plexiform layer. Glycine receptor mRNAs were found in the inner nuclear layer and the ganglion cell layer. The α 1 subunit mRNA is predominantly present in the outer half of the INL and on some but not all ganglion cells. GlyR α2 subunit mRNA is predominantly present in the inner half of the INL and on nearly all cells in the ganglion cell layer. GlyR α3–, GlyR β-, and gephyrin-mRNAs are present in the entire INL and in cells in the ganglion cell layer. The differential expression of glycine receptor subunits indicates a functional diversity of glycine receptors in the retina.


2003 ◽  
Vol 20 (4) ◽  
pp. 373-384 ◽  
Author(s):  
THOMAS C. ROTOLO ◽  
RAMON F. DACHEUX

The major inhibitory neurotransmitters GABA and glycine provide the bulk of input to large-field ganglion cells in the retina. Whole-cell patch-clamp recordings were used to characterize the glycine- and GABA-activated currents for morphologically identified ON-α ganglion cells in the rabbit retina. Cells identified as ON-α cells by light evoked currents were intracellularly stained and examined by light microscopy which revealed dendritic stratification in the vitreal half of the inner plexiform layer and confirmed their physiological identity. All Ca2+-mediated synaptic influences were abolished with Co2+, revealing two types of ON-α cell characterized by their different inhibitory current profiles. One group exhibited larger glycine- than GABA-activated currents, while the other group had larger GABA- than glycine-activated currents. Both cell types demonstrated strychnine-sensitive glycine-activated currents and bicuculline-sensitive GABAA-activated currents. Surprisingly, both cell types expressed functional GABAC receptors demonstrated by their sensitivity to TPMPA. In addition, the cells with larger glycine-activated currents also possessed GABAB receptors, whereas those with larger GABA-activated currents did not. Immunocytochemical experiments confirmed the presence of glycine, GABAA, and GABAC receptor subunits on all physiologically identified ON-α ganglion cells in this study. In addition, the GABAB receptor immunolabeled puncta were present on the cells with larger glycine-activated currents, but not on the cells with the larger GABA-activated currents. In conclusion, the presence of different functional GABA and glycine receptors determined physiologically correlated well with the specific GABA and glycine receptor immunolabeling for two neuropharmacological types of rabbit ON-α ganglion cells.


1979 ◽  
Vol 83 (1) ◽  
pp. 159-178 ◽  
Author(s):  
R H Masland ◽  
J W Mills

Rabbit retinas were studied in vitro under conditions known to maintain their physiological function. Retinas incubated in the presence of [3H]choline synthesized substantial amounts of both [3H]phosphorylcholine and [3H]acetylcholine. With time, [3H]phosphorylcholine proceeded into phospholipids, primarily phosphatidylcholine. Retinas pulse-labeled by a 15-min exposure to 0.3 microM [3H]choline were incubated for a subsequent hour under chase conditions designed either to retain newly synthesized acetylcholine within synapses or to promote its release. At the end of this time the two groups of retinas were found to contain equal amounts of radioactivity in the phospholipid pathway, but only the retinas incubated under the acetylcholine-protecting conditions contained [3H]acetylcholine. Freeze-dried, vacuum-embedded tissue from each retina was autoradiographed on dry emulsion. All retinas showed silver grains over the photoreceptor cells and faint labeling of all ganglion cells. In the retinas that contained [3H]acetylcholine, silver grains also accumulated densely over a few cells with the position of amacrine cells, over a subset of the cells of the ganglion cell layer, and in two bands over the inner plexiform layer. Fixation of the retina with aqueous osmium tetroxide retained only the radioactive compounds located in the photoreceptor and ganglion cells. Sections from freeze-dried tissue lost their water-soluble choline metabolites when exposed to water, and autoradiography of such sections again revealed radioactivity primarily in the photoreceptor and ganglion cells. Radioactive compounds extracted from the sections were found to faithfully reflect those present in the tissue before processing; analysis of the compounds eluted from sections microdissected along the outer plexiform layer showed [3H]acetylcholine to have been synthesized only by cells of the inner retina. Taken together, these results indicate that the photoreceptor and ganglion cells are distinguished by a rapid synthesis of choline-containing phospholipids, while acetylcholine synthesis is restricted to a few cells at both margins of the inner plexiform layer. They imply that the only neurons to release acetylcholine within the rabbit retina are a small group of probable amacrine cells.


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