Feedback connections and operation of the outer plexiform layer of the retina.

The primary feedback control apparatus in the outer retina is the sign-inverting feedback synapse between horizontal cells and cones. In many lower vertebrates horizontal cells release GABA in darkness, which opens Cl- channels in cones. Input-output relations of the feedback synapse reveal that the synaptic gain is light-dependent with the highest negative gain near the dark horizontal cell potential. The horizontal cell-cone feedback synapse improves the reliability of the photoreceptor output synapses. It also modulates the dynamic range and mediates color opponency and surround responses in second-order retinal neurons.     

Neuronal and synaptic organization of the outer plexiform layer of the pigeon retina

The organization of the outer plexiform layer (OPL) of the pigeon retina is described by electron microscopy and Golgi impregnation. Six types of photoreceptor, four types of horizontal cell, eight types of bipolar cell, and an interplexiform cell type were found by Golgi impregnation. The OPL was tri-stratified due to the endings of the photoreceptors at three different levels. This stratification was reflected in the laminar arrangement of the dendrites of the horizontal and bipolar cells. Electron microscopy showed that the synaptic endings of the photoreceptors made ribbon synapses, both triads and dyads, and basal junctions with the process of second-order neurons. Horizontal cells formed conventional chemical synapses, while horizontal cell axon terminals were extensively linked by gap junctions.     

Localization of metabotropic glutamate receptors in the outer plexiform layer of the goldfish retina

We studied the localization of metabotropic glutamate receptors (mGluRs) in the goldfish outer plexiform layer by light-and electron-microscopical immunohistochemistry. The mGluR1α antibody labeled putative ON-type bipolar cell dendrites and horizontal cell processes in both rod spherules and cone triads. Immunolabeling for mGluR2/3 was absent in the rod synaptic complex but was found at horizontal cell dendrites directly opposing the cone synaptic ribbon. The mGluR5 antibody labeled Müller cell processes wrapping rod terminals and horizontal cell somata. The mGluR7 antibody labeled mainly horizontal cell dendrites invaginating rods and cones and some putative bipolar cell dendrites in the cone synaptic complex. The finding of abundant expression of various mGluRs in bipolar and horizontal cell dendrites suggests multiple sites of glutamatergic modulation in the outer retina. Financial support for this work was provided by Conselho Nacional de Pesquisa (CNPq), Brazil (grant 200915/98-3 to C.J.)     

Ectopic localization of putative AII amacrine cells in the outer plexiform layer of the developing FVB/N mouse retina

The FVB/N mouse is a model of retinitis pigmentosa which shows a rapid loss of photoreceptors during early postnatal (P) life. We investigated the cellular localization of glycine transporter 1 (GlyT-1) in the developing FVB/N mouse retina. In control retinas, the developmental pattern of GlyT-1-immunoreactive amacrine cells was well in accordance with a previous report. However, in the FVB/N mouse retina, some GlyT-1-labeled amacrine cells sent their processes into the outer plexiform layer (OPL) from P14 onward. From P21 onward, GlyT-1-labeled cells were visible in the OPL. These cells were further characterized by double-label immunofluorescence experiments with an antiserum against disabled 1 (Dab-1), and showed Dab-1 immunoreactivity, indicating that these cells are putative AII amacrine cells. These results clearly demonstrate that AII amacrine cells have the potential capacity to respond to photoreceptor degeneration by migrating or sprouting their processes into the OPL in the developing FVB/N mouse retina.This study was supported by a Korea Research Foundation Grant (2001, PF0005) from the Ministry of Education     

Phase-contrast microscopy of the primate retina

The study of hematoxylin and eosin stained thick sections (15 microns) of the primate retina with the phase-contrast microscope provided a means for the selective demonstration of many cellular structures that could not be resolved with the same degree of detail which was possible when bright-field microscopy was used, or when phase-contrast microscopy was employed to examine unstained material. The H & E-stain greatly enhanced the phase-contrast image, so that cytoplasmic structure, fiber trajectories, and gross synaptic detail of the retina could be demonstrated to better advantage.     

The ramification pattern of amacrine cells within the inner plexiform layer of the carp retina

Summary The morphology of amacrine cells in the retina of the carp is described using the Golgi technique. The ramification pattern of these cells was analyzed in flat-mounts of retinas. Based on these observations classification into five groups was made. Cells possessing one principal process leaving the soma were subdivided into starburst A-neurons and radiate neurons. Cells having two or more principal processes were subdivided into starburst B-neurons and spindle-shaped soma neurons. Small, diffuse amacrine cells form the fifth group. With respect to the shape of the field of arborization, the following cell types could be distinguished: (i) uniform cells, (ii) cells with a preferential direction, and (iii) cells with a marked edge, i.e., cells that lack processes in one direction. The latter form rarely occurs among starburst neurons; most of the spindle-shaped soma cells possess processes with a preferred direction, and cells with a marked edge are mainly found among the radiate neurons.All five cell types are found throughout the retina. The size of the cells varies within each group, and there is no correlation between size and distance from the optic nerve.The radial arborization pattern of each cell was examined in serial transverse sections. Starburst A-neurons ramify in the middle of the inner plexiform layer (IPL), radiate neurons in the inner half, and spindle-shaped soma neurons without overlapping processes (type B) as well as starburst B-neurons in the outer half. The ramification can be monostratified (narrow or broad), bistratified or multistratified. Small, diffuse amacrine cells and spindle-shaped soma neurons with overlapping processes (type A) ramify throughout the entire IPL.This work was supported by the Deutsche Forschungsgemeinschaft     

Some horizontal cells of the bovine retina receive input synapses in the inner plexiform layer

Bovine retinae were stained immunocytochemically with antibodies against the calcium-binding protein, calbindin. Horizontal cells in the outer plexiform layer were heavily labelled. The processes of most horizontal cells were confined to the level of the outer plexiform layer, and the tips of their dendrites were positioned as the lateral elements of the cone triads, viz. the usual mammalian arrangement. However, some of the horizontal cells had additional thick processes descending to branch within the inner plexiform layer, where they were postsynaptic at bipolar cell dyads and where they also received input from amacrine cells. No output synapses of horizontal cells were observed in the inner plexiform layer.     

Synaptic connections of calbindin-immunoreactive cone bipolar cells in the inner plexiform layer of rabbit retina

In the mammalian retina, information concerning various aspects of an image is transferred in parallel, and cone bipolar cells are thought to play a major role in this parallel processing. We have examined the synaptic connections of calbindin-immunoreactive (IR) ON cone bipolar cells in the inner plexiform layer (IPL) of rabbit retina and have compared these synaptic connections with those that we have previously described for neurokinin 1 (NK1) receptor-IR cone bipolar cells. A total of 325 synapses made by calbindin-IR bipolar axon terminals have been identified in sublamina b of the IPL. The axons of calbindin-IR bipolar cells receive synaptic inputs from amacrine cells through conventional synapses and are coupled to putative AII amacrine cells via gap junctions. The major output from calbindin-IR bipolar cells is to amacrine cell processes. These data resemble our findings for NK1 receptor-IR bipolar cells. However, the incidences of output synapses to ganglion cell dendrites of calbindin-IR bipolar cells are higher compared with the NK1-receptor-IR bipolar cells. On the basis of stratification level and synaptic connections, calbindin-IR ON cone bipolar cells might thus play an important role in the processing of various visual aspects, such as contrast, orientation, and approach sensing, and in transferring rod signals to the ON cone pathway.     

Serotonin systems in the inner and outer plexiform layers of the vertebrate retina

In retinas of certain nonmammalian vertebrate species such as frog, pigeon, and chick, serotonin appears to function as the neurotransmitter of a specific population of amacrine cells. Neurochemical and morphological studies have demonstrated high endogenous levels of 5-hydroxytryptamine (5-HT) as well as uptake, release, and receptor-binding activity restricted to the inner plexiform layer. In retinas from most mammalian species, uptake, release, and receptor-binding activity have also been localized to amacrine cell terminals in the inner plexiform layer. However, serotonin content in mammalian retinas is low, and attempts to localize the endogenous store of 5-HT have failed. Thus the status of serotonin as a candidate in mammalian retina is still open to question. Our more recent studies have revealed a light-sensitive serotonin system associated with photoreceptor terminals in retinas of Long-Evans rats. Uptake, synthesis, and release of [3H]serotonin have been demonstrated. Endogenous levels of 5-HT decrease in the dark and increase in the light. Electrophysiological studies are needed to illucidate the functional role(s) of serotonin within retinas of different species.     

Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits

Freeze-fracture analysis of the neural connections in the outer plexiform layer of the retina of primates (Macaca mulatta and Macaca arctoides) demonstrates a remarkable diversity in the internal structure of the synaptic membranes. In the invaginating synapses of cone pedicles, the plasma membrane of the photoreceptor ending contains an aggregate of A-face particles, a hexagonal array of synaptic vesicle sites, and rows of coated vesicle sites, which are deployed in sequence from apex to base of the synaptic ridge. The horizontal cell dendrites lack vesicle sites and have two aggregates of intramembrane A-face particles, one at the interface with the apex of the synaptic ridge, the other opposite the tip of the invaginating midget bipolar dendrite. Furthermore, the horizontal cell dendrites are interconnected by a novel type of specialized junction, characterized by: (a) enlarged intercellular cleft, bisected by a dense plate and traversed by uniformly spaced crossbars; (b) symmetrical arrays of B-face particles arranged in parallel rows within the junctional membranes; and (c) a layer of dense material on the cytoplasmic surface of the membranes. The plasmalemma of the invaginating midget bipolar dendrite is unspecialized. At the contact region between the basal surface of cone pedicles and the dendrites of the flat midget and diffuse cone bipolar cells, the pedicle membrane has moderately clustered A-face particles, but no vesicle sites, whereas the adjoining membrane of the bipolar dendrites contains an aggregate of B-face particles. The invaginating synapse of rod spherules differs from that of cone pedicles, because the membrane of the axonal endings of the horizontal cells only has an A-face particle aggregate opposite the apex of the synaptic ridge. Specialized junctions between horizontal cell processes, characterized by symmetrical arrays of intramembrane B-face particles, are also present in the neuropil underlying the photoreceptor endings. Small gap junctions connect the processes of the horizontal cells; other gap junctions probably connect the bipolar cell dendrites which make contact with each cone pedicle. Most of the junctional specializations typical of the primate outer plexiform layer are also found in the rabbit retina. The fact that specialized contacts between different types of neurons interacting in the outer plexiform layer have specific arrangements of intramembrane particles strongly suggests that the internal structure of the synaptic membranes is intimately correlated with synaptic function.