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

1975 ◽  
Vol 65 (1) ◽  
pp. 192-222 ◽  
Author(s):  
E Raviola ◽  
N B Gilula

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.

2000 ◽  
Vol 17 (2) ◽  
pp. 255-262 ◽  
Author(s):  
DIANNA A. JOHNSON ◽  
STEPHEN L. MILLS ◽  
MICHAEL F. HABERECHT ◽  
STEPHEN C. MASSEY

In the mature rabbit retina, two classes of horizontal cells, A type and B type, provide lateral inhibition in the outer plexiform layer (OPL) and spatially modify the activation of bipolar cells by photoreceptors. Gap junctions connecting homologous horizontal cells determine the extent to which this inhibitory activity spreads laterally across the OPL. Little is currently known about the expression of gap junctions in horizontal cells during postnatal development or how cell–cell coupling might contribute to subsequent maturational events. We have examined the morphological attributes and coupling properties of developing A and B type horizontal cells in neonatal rabbit retina using intracellular injections of Lucifer Yellow and Neurobiotin. Prelabeling with DAPI permitted the targeting of horizontal cell bodies for intracellular injection in perfused preparations of isolated retina. A and B type horizontal cells were identifiable at birth although their dendritic field sizes had not reached adult proportions and their synaptic contacts in the OPL were minimal. Both cell types exhibited homologous dye coupling at birth. Similar to that seen in the adult, no heterologous coupling was observed, and homologous coupling among A type cells was stronger than that observed among B type cells. The spread of tracer compounds through gap junctions of morphologically immature horizontal cells suggests that ions and other small, bioactive compounds may likewise spread through coupled, horizontal networks to coordinate the subsequent maturational of emerging outer plexiform layer pathways.


1987 ◽  
Vol 229 (1257) ◽  
pp. 345-379 ◽  

The presence in the rhesus monkey’s retina of a second morphological type of horizontal cell (H2), described by Kolb et al . (1980), is confirmed. Both types of cell are here further described. Their cone connections are quantified and compared with those of mammals and other vertebrates. The dendrites and axons of the H2 type of cell contact only cones as do the dendrites of the H1 cell (originally described by Polyak (1941)) which has an axon contacting only rods. The dendrites of foveal H2 cells contact between 11 and 14 cones; those of H1 contact 7. The number of cones that each type of cell contacts increases with increasing distance from the fovea, so that, by 5-6 mm eccentricity, H2-type cells synapse with between 20 and 30 cones, and the H1 cells with 12-15. The qualitatively estimated coverage factors of each are 3 or 4; every cone synapses with more than one of both types. Neither type of horizontal cell makes chromatically specific connections that are anatomically recognizable, unlike the situation in some teleostean and turtle retinae. Individual horizontal cells, particularly those connected to foveal cones, may have different ratios of chromatic input. At equivalent eccentricities, up to about 6 mm from the fovea, the dendritic fields of H2 horizontal cells are about twice the size of H1 cells and contact about twice the number of cones. These relative differences are closely similar to those of the cat’s horizontal cells and it is suggested that they are a basic feature of most placental mammals. The organization of foveal cone fibres within Henle’s layer is described. The distribution of primate cone telodendria, gap junctions and synapses in the outer plexiform layer are briefly reviewed and compared with those of other vertebrate retinae.


1974 ◽  
Vol 186 (1085) ◽  
pp. 317-331 ◽  

Two ultrastructurally distinctive types of horizontal cells are described in the retinae of the cat and the rabbit. Evidence is presented that they have different synaptic connexions in the outer plexiform layer. The majority of the presynaptic structures identified in the outer plexiform layer of the rabbit (as defined on page 320) belong to a neurofilamentous type of horizontal cell. It is suggested that the cat may be the same. No synapses have been identified on to, or from, the second, predominantly neurotubular, type of horizontal cell. No chemical synapses on to, or between, horizontal cells have been found. Thus input of this kind to both types of horizontal cells is as yet only known to be from the photoreceptors. All positively identified postsynaptic processes were the dendrites or perikarya of bipolar cells. Other cell types that are possibly pre- or postsynaptic in the outer plexiform layer are discussed.


The intercellular junctions of cone pedicles in the turtle retina were studied electronmicroscopically in tissue prepared by conventional techniques or impregnated by the method of Golgi. Dendritic branchlets of bipolar cells make specialized contacts with the basal surface of the pedicles. Processes ending laterally to wedge-shaped projections (synaptic ridges) of the pedicles probably belong always to horizontal cells, and make proximal and distal (to the synaptic ridges) junctions with the pedicles. Processes ending opposite the apex of the synaptic ridges are engaged also in two kinds of specialized contacts, termed apical and distal junctions. Basal processes of the cone pedicles make specialized contacts with adjacent pedicles, and with unidentified processes at the outer plexiform layer; their endings abut upon horizontal cell processes lodged within the pedicles of other cone cells.


1996 ◽  
Vol 76 (4) ◽  
pp. 2307-2315 ◽  
Author(s):  
D. G. McMahon ◽  
L. V. Ponomareva

1. In the retina, as in other regions of the vertebrate central nervous system, glutamate receptors mediate excitatory chemical synaptic transmission and are a critical site for the regulation of cellular communication. In this study, retinal horizontal cells from the hybrid less were dissociated in cell culture, voltage clamped by the whole cell recording technique, and the currents evoked by application of excitatory amino acids recorded. 2. Responses to glutamate and its agonist kainate were reduced by approximately 50% in the presence of the nitric oxide (NO) donors sodium nitroprusside and S-nitroso-N-acetylpenicillamine. The effect of these compounds was blocked by the NO scavenger hemoglobin. 3. This effect of NO donors on kainate currents could be mimicked by the application of a membrane permeable guanosine 3',5'-cyclic monophosphate (cGMP) analogue, 8-Br-cGMP. The NO effect was also blocked by application of the guanylate cyclase inhibitor LY-83583, and by a protein kinase G inhibitor peptide. 4. In H1-type horizontal cells, stimulation of endogenous nitric oxide synthase with L-arginine reduced kainate responses, whereas application of D-arginine had no effect. 5. This receptor modulation mechanism may act in concert with other pre- and postsynaptic mechanisms to modify horizontal cell synaptic function according to the adaptational state of the retina and also may protect horizontal cells from glutamate excitotoxicity.


1974 ◽  
Vol 63 (1) ◽  
pp. 62-87 ◽  
Author(s):  
Frank S. Werblin

Test stimuli, presented at the center of the bipolar cell receptive field, spanning less than 2 log units of intensity, elicit the full range of graded response. The intensity range of test stimuli that elicits the graded response depends upon the background conditions. A higher range of log test intensities is required to elicit the graded bipolar response in the presence of surround backgrounds. But surround backgrounds can also serve to unsaturate the bipolar response and thereby increase sensitivity under certain conditions. The results suggest that a second stage of sensitivity-control is mediated by the horizontal cell system at the outer plexiform layer, concatenated with the effects of adaptation in the photoreceptors.


1990 ◽  
Vol 64 (2) ◽  
pp. 313-325 ◽  
Author(s):  
R. Pflug ◽  
R. Nelson ◽  
P. K. Ahnelt

1. Dim backgrounds can enhance small-spot flicker responses of cat retinal horizontal cells by a factor of 2 or more. 2. Intracellular marking with horseradish peroxidase (HRP) reveals that this enhancement effect occurs in--but is not necessarily limited to--the cone-connected, A-type horizontal cell. 3. Flicker amplitudes decrease over a frequency range from 3 to 36 Hz of square-wave photic stimulation. There is little evidence of flicker-response enhancement at 3 Hz. Flicker-response enhancement is typically 2-6 times larger at 35 than at 6 Hz. 4. Inspection of flicker waveforms indicates both a scaling-up of response signals with backgrounds and a distortion composed of 2- to 5-ms-latency decrease, expressed primarily within a quick component of OFF-repolarization. 5. Flicker enhancement first increases as a function of background irradiance and then decreases. The increasing limb has the dynamic range and spectral sensitivity of cat rods (507-nm peak). Enhancement is maintained during rod after-effects. The decreasing limb of the background-versus-intensity function results from light adaptation of cat, long-wavelength (red) cones. 6. The flicker responses themselves peak spectrally at approximately 555 nm and reflect only the activity of cat long-wavelength (red) cones, without evidence of intermixing of other photoreceptor mechanisms. 7. Thus within the first synaptic layer of the cat visual system, rod signals interact with the flicker responses of red cones, both increasing cone-signal amplitudes and modifying cone-signal waveforms. 8. The results are closely analogous to "suppressive rod-cone interaction" (SRCI) as described in human psychophysics. 9. An outer-plexiform-layer circuit involving rods, horizontal cells and cones may mediate rod-induced enhancement of cone flicker. This being the case, notions of horizontal-cell feedback interactions with cones may have to be modified and extended. A specific feedback model is elaborated in the companion paper.


1995 ◽  
Vol 12 (5) ◽  
pp. 985-999 ◽  
Author(s):  
Stewart A. Bloomfield ◽  
Daiyan Xin ◽  
Seth E. Persky

AbstractThe large receptive fields of retinal horizontal cells are thought to reflect extensive electrical coupling via gap junctions. It was shown recently that the biotinylated tracers, biocytin and Neurobiotin, provide remarkable images of coupling between many types of retinal neuron, including horizontal cells. Further, these demonstrations of tracer coupling between horizontal cells rivaled the size of their receptive fields, suggesting that the pattern of tracer coupling may provide some index of the extent of electrical coupling. We studied this question by comparing the receptive field and tracer coupling size of dark-adapted horizontal cells recorded in the superfused, isolated retina-eyecup of the rabbit. Both the edge-to-edge receptive field and space constants (λ) were computed for each cell using a long, narrow slit of light displaced across the retinal surface. Cells were subsequently labeled by iontophoretic injection of Neurobiotin. The axonless A-type horizontal cells showed extensive, homologous tracer coupling in groups greater than 1000 covering distances averaging about 2 mm. The axon-bearing B-type horizontal cells were less extensively tracer coupled, showing homologous coupling of the somatic endings in groups of about 100 cells spanning approximately 400 μm and a separate homologous coupling of the axon terminal endings covering only about 275 μm. Moreover, we observed a remarkable, linear relationship between the size of the receptive fields of each of the three horizontal cell endings and the magnitude of their tracer coupling. Our findings suggest that the extent of tracer coupling provides a strong, linear index of the magnitude of electrical current flow, as derived from receptive-field measures, across groups of coupled horizontal cells. These data thus provide the first direct evidence that the receptive-field size of horizontal cells is related to the extent of their coupling via gap junctions.


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