Parasol Ganglion Cells Research Articles

Distribution of the alpha1 subunit of the GABA(A) receptor on midget and parasol ganglion cells in the retina of the common marmoset Callithrix jacchus.

The inhibitory neurotransmitter gamma aminobutyric acid (GABA) has been shown to influence the responses of ganglion cells in the mammalian retina. Consistently, GABA(A) receptor subunits have been localized to different ganglion cell types. In this study, the distribution of the alpha1 subunit of the GABA(A) 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 alpha1 subunit of the GABA(A) 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/microm dendrite) than midget cells (0.054 puncta/microm dendrite).

Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina.

In primate retinas, the dendrites of DB3 diffuse bipolar cells are known to receive inputs from cones. The goal of this study was to describe the synaptic connections of DB3 bipolar cell axons in the inner plexiform layer. DB3 bipolar cells in midperipheral retina were labeled with antibodies to calbindin, and their axons were analyzed in serial, ultrathin sections by electron microscopy. Synapses were found almost exclusively at the axonal varicosities of DB3 axon terminals. There were 2.14 synaptic ribbons per varicosity. There were 33 varicosities per DB3 cell, giving an average of 71 ribbons per axon terminal. Because there were 1.5 postsynaptic ganglion cell dendrites per DB3 axonal varicosity, we estimate that there is at least 1 synapse per varicosity onto a parasol ganglion cell dendrite. There were 3.4 input synapses from amacrine cells per axonal varicosity. Among these were feedback synapses to the DB3 bipolar cell axon varicosities, which were made by 47% of the postsynaptic amacrine cell processes. Some of the feedback synapses could be from amacrine cells immunoreactive for cholecystokinin precursor or choline acetyltransferase, because both types of amacrine cells costratify with parasol cells and are known to be presynaptic to bipolar cells. AII amacrine cells were both presynaptic and postsynaptic to DB3 axons, a finding consistent with the large rod input to parasol ganglion cells reported in physiological experiments. DB3 bipolar cell axons also made frequent contacts with neighboring DB3 axons, and gap junctions were always found at these sites.

Midget and parasol ganglion cells of the primate retina express the alpha1 subunit of the glycine receptor.

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 alpha1 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 alpha1 subunit of the glycine receptor.

Morphological analysis of the blue cone pathway in the retina of a New World monkey, the marmosetCallithrix jacchus

We have studied the components of the short wavelength-sensitive (SWS or "blue") cone pathway in the retina of a New World primate, the marmoset Callithrix jacchus. Of particular interest was the small bistratified ganglion cell, which has been identified in macaque monkey to be the morphological substrate of the blue-ON cell (Dacey and Lee [1994] Nature 367:731-735). Small bistratified cells were intracellularly filled with Neurobiotin in an in vitro retinal wholemount preparation. Their morphology, size, and level of dendritic stratification were similar to their homologues in macaque and human retina. A number of different antibodies were applied to vertical cryostat sections, some of which were cut through the processes of injected small bistratified or parasol ganglion cells. We used antibodies against cholecystokinin (CCK) to label blue cone bipolar cells, and antibodies against the human SWS cone photopigment to label SWS cones. Double-labelled preparations showed that blue cone bipolar cell dendrites contact SWS cone pedicles, and the inner dendrites of the small bistratified cell are costratified with the axon terminals of blue cone bipolar cells. A monoclonal antibody against calbindin was used to label a subpopulation of bipolar cells that stratifies in the outer half of the inner plexiform layer. The axon terminals of these bipolar cells occasionally cross the outer dendrites of small bistratified cells and show extensive costratification with the dendrites of OFF parasol cells. We conclude that an SWS cone pathway with similar connectivity is a preserved feature of the primate visual system.

Synaptic Inputs to ON Parasol Ganglion Cells in the Primate Retina

In primates, the retinal ganglion cells that project to the magnocellular layers of the lateral geniculate nucleus have distinctive responses to light, and one of these has been identified morphologically as the parasol ganglion cell. To investigate their synaptic connections, we injected parasol cells with Neurobiotin in lightly fixed baboon retinas. The five ON-center cells we analyzed by electron microscopy received approximately 20% of their input from bipolar cells. The major synaptic input to parasol cells was from amacrine cells via conventional synapses and, in this respect, they resembled alpha ganglion cells of the cat retina. We also found the gap junctions between amacrine cells and parasol ganglion cells that had been predicted from tracer-coupling experiments. To identify the presynaptic amacrine cells, ON-center parasol cells were injected with Neurobiotin and Lucifer yellow in living macaque retinas, which were then fixed and labeled by immunofluorescence. Two kinds of amacrine cells were filled with Neurobiotin via gap junctions: a large, polyaxonal cell containing cholecystokinin and a smaller one without cholecystokinin. There were also appositions between cholecystokinin-containing amacrine cell processes and parasol cell dendrites. Cholinergic amacrine cell processes often followed parasol cell dendrites and made extensive contacts. In other mammals, the light responses of polyaxonal amacrine cells like these and cholinergic amacrine cells have been recorded, and the effects of acetylcholine and cholecystokinin on ganglion cells are known. Using this information, we developed a model of parasol cells that accounts for some properties of their light responses.

Parasol (Pα) ganglion-cells of the primate fovea: Immunocytochemical staining with antibodies against GABA A-receptors

Retinae of macaque monkeys were immuno-stained with antibodies against GABA A-receptors. In peripheral retina most ganglion cells were immunoreactive. In central retina, around the fovea, staining in the ganglion cell layer was selective and only 5–8% of all ganglion cells were labelled: these had the largest cell bodies and their dendrites occupied a broad stratum in the middle of the inner plexiform layer. From comparison with Golgi-stained ganglion cells it is concluded that the entire population of parasol (Pα)-cells at the fovea was labelled. The mosaic and sampling properties of parasol cells were determined by combining dendritic field measurements of Golgi-stained cells with their density when immuno-stained. There is convergence of 30–50 cones onto each foveal parasol ganglion cell. The dendritic fields of both ON- and OFF-parasol cells provide complete retinal coverage. The Nyquist limits of their mosaics are 4 min of arc.

POSTMORTEM PRESERVATION OF GANGLION CELLS IN THE HUMAN RETINA

Postmortem morphometric investigation of autopsy material is helpful for understanding the alterations cells undergo during life. The present work was undertaken to determine the morphologic features of human retinal ganglion cells during the first 2 days after death. Ganglion cells of 16 retinas were obtained from eyes, the corneas of which had been retrieved for keratoplasties. The ganglion cells were stained with the fluorescent carbocyanine dye Dil and investigated 12 to 36 hours postmortem. All labeled cells identified as ganglion cells had well preserved, type-specific dendritic profiles that made it possible to catalog them according to the established classes of ganglion cells. The various types of cells have in common some typical morphologic changes that occur during the postmortem period of observation: swelling and varicosity in the cell bodies and along the dendritic branches and the axons. These swellings were consistent throughout the postmortem period and did not hinder the identification of particular types of ganglion cells. The two major types (parasol and midget) and various subtypes of ganglion cells were identified morphologically. There are two distinct morphologic types of midget cells which differ from each other in the pattern of dendritic branching. Particular emphasis was given to analyze the dendritic geometry of the large parasol cells. A new finding in the human retina is the frequent presence of large parasol ganglion cells, the axons of which course along aberrant intraretinal paths, especially in the extreme periphery of the retina.

Distribution of GABA-immunoreactive amacrine cell synapses in the inner plexiform layer of macaque monkey retina

The distribution patterns of GABA immunoreactive (+) and immunonegative (-) amacrine cell synapses and profiles in the inner plexiform layer (IPL) were analyzed in three macaque monkey retinas using postembedding electron-microscopic (EM) immunogold cytochemistry. Synapses and profiles were counted at 5% intervals throughout the IPL depth in three EM montages (total area = 6509 microns 2), with 0% depth at the inner nuclear layer/IPL border. Nearly 70% of all amacrine synapses were GABA+, and they contacted all major classes of neurons that arborize in the IPL: bipolars (45%), ganglion cells (25%), and GABA+ (20%) and GABA- (10%) amacrines. A major relationship was seen between GABA+ amacrine processes and bipolar terminals: 76% of all amacrine-to-bipolar synapses were GABA+, and 82% of bipolar output dyads contained at least one GABA+ amacrine. GABA+ amacrine profiles (N = 2455) were concentrated in three wide bands at IPL depths of 0-25%, 40-60%, and 75-100%, corresponding to the dense bands seen with light-microscopic immunocytochemistry. In contrast, GABA+ amacrine synapses (N = 1081) were distributed evenly throughout the IPL depth, rather than being confined to the three dense bands. GABA- amacrine synapses (N = 516) were concentrated at 40% and 60% depths. Each category of amacrine output synapses had a characteristic pattern of stratification in the IPL. GABA+ amacrine-to-bipolar synapses occurred throughout the IPL but were most frequent at 20% and 80% IPL depths, where the dendrites of midget cone bipolars arborize (Polyak, 1941). In contrast, GABA+ amacrine-to-ganglion cell synapses were concentrated at 30% and 70% IPL depths, near the dendritic arborizations of parasol ganglion cells (Watanabe & Rodieck, 1989). GABA+ synapses onto bipolars and amacrines were also concentrated at the level of rod bipolar terminals. GABA+ amacrines must play significant but different roles in ON and OFF midget and parasol pathways as well as the rod pathway.

Parasol and midget ganglion cells of the primate retina

We have intracellularly filled the dendritic arbors of 996 midget and parasol ganglion cells with horseradish peroxidase (HRP) in macaque and baboon retinas. Only minor differences in the properties of these cell groups were found between species. Ninety of these cells were cut from their retinas, embedded in methacrylate, and transversely sectioned. According to their depth of stratification, there are two types of parasol cells (termed a-parasol and b-parasol), and two types of midget ganglion cells (a-midget and b-midget). Each of these four types stratifies at a different level within the IPL. The dendritic fields of midget ganglion cells lie either near the border of the ganglion cell layer (GCL) or near the border of the amacrine cell layer (ACL). The dendrites of the two types of parasol cells stratify closer to the center of the IPL, where they divide it into three approximately equal parts. There was no vertical overlap in the dendritic fields of a-parasols and b-parasols; they were always separated by at least 1 micron. The border between the a- and b-sublaminae of the IPL, defined in terms of this narrow gap between the stratification of the two parasol cell types, lies approximately at the center of the IPL. The dendritic-field thickness for each of these types, on average, is no greater than 30% of the IPL thickness. At a similar location, there is no significant difference between the dendritic-field diameters of the two parasol types or between those of the two midget types. As previously reported (Perry et al.: Neuroscience 12:1101-1123, '84) the dendritic fields of both parasol and midget ganglion cells are smaller in the nasal retina than at a position in the temporal retina equidistant from the fovea. Because dendritic-field diameters prove to depend upon local ganglion-cell density, the scatter in these diameters as a function of retinal eccentricity is due in part to the asymmetric distribution of ganglion cells. We have devised a measure, termed equivalent eccentricity, that allows data points of cells from regions having the same local ganglion-cell density to be plotted at the same position on this scale. The use of this measure, rather than eccentricity per se, significantly reduces the scatter of dendritic-field diameters. The dendritic-field diameters of parasol cells within the nasal quadrant of the retina are not fully brought into line with those of cells lying elsewhere in the retina.(ABSTRACT TRUNCATED AT 400 WORDS)

Morphological analysis of parasol and midget ganglion cells in primate retinas

Morphological analysis of parasol and midget ganglion cells in primate retinas