Synaptic organization of cone cells in the turtle retina

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.

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 effects of atomized solutions of dopamine and certain related com­pounds have been tested on the intracellularly recorded activity of receptor, horizontal, bipolar and amacrine cells in the goldfish retina. Dopamine depolarizes the cone L-type horizontal cells and reduces the amplitude of light-evoked responses. These effects on L-type horizontal cells are completely abolished by the α-adrenergie blocker, phentolamine, but only partially depressed by the β-blocker, propanolol. L-Dopa, noradrenalin, and serotonin do not have effects on L-type horizontal cells when applied at concentrations similar to those that cause maximal dopamine effects. The results suggest that the effects of dopamine on L-type horizontal cells are specific, and we propose that they mimic the effects of interplexiform cell activity. Dopamine has no effects on rod horizontal cells in goldfish and variable effects on C-type horizontal cells. On bipolar cells, dopamine alters the dark membrane potential, enhances the central response to light, and depresses the surround response. Dopamine also decreases the horizontal cell feedback evident in cone responses. Finally, dopamine strongly depolarizes the transient type of amacrine cells, but it has no significant effect on the sustained type of amacrine cells. Assuming that dopamine is the transmitter of interplexiform cells, we suggest that these neurons regulate lateral inhibitory effects mediated by L-type horizontal cells in the outer plexiform layer and transient amacrine cells in the inner plexiform layer. In addition, it appears as if interplexiform cells have specific effects on bipolar cells and are capable of regulating centre-surround antagonism in these cells. The net effect of interplexiform cell activity is to isolate the bipolars from the influence of the surround.


1981 ◽  
Vol 211 (1184) ◽  
pp. 373-389 ◽  

A serial section analysis of photoreceptor synaptic bases was undertaken in the clawed frog Xenopus laevis . The developmental period from tadpole stage 48 through metamorphosis was studied. Horizontal cells contacted rod and cone photoreceptors at ribbon synapses; the number of such contacts per receptor base was constant for rods, but increased for cones as a function-of developmental stage. In pre-metamorphic animals bipolar cells contacted receptors only through basal junctions; their number in cone bases increased dramatically during development but was unchanged in rod bases. A densitometric estimation of the cleft width of basal junctions showed that it ranged from 10 to 18 nm, but the junctions could not be divided reliably into the ‘wide’ and ‘narrow’ categories reported for other vertebrate species. Near metamorphic climax a new type of ribbon-related bipolar cell junction appeared. Gap junctions between horizontal cells and conventional chemical synapses of horizontal cell onto bipolar cell processes were first seen in mid-larval developmental stages.


2007 ◽  
Vol 24 (4) ◽  
pp. 489-502 ◽  
Author(s):  
ARLENE A. HIRANO ◽  
JOHANN HELMUT BRANDSTÄTTER ◽  
ALEJANDRO VILA ◽  
NICHOLAS C. BRECHA

Horizontal cells mediate inhibitory feed-forward and feedback communication in the outer retina; however, mechanisms that underlie transmitter release from mammalian horizontal cells are poorly understood. Toward determining whether the molecular machinery for exocytosis is present in horizontal cells, we investigated the localization of syntaxin-4, a SNARE protein involved in targeting vesicles to the plasma membrane, in mouse, rat, and rabbit retinae using immunocytochemistry. We report robust expression of syntaxin-4 in the outer plexiform layer of all three species. Syntaxin-4 occurred in processes and tips of horizontal cells, with regularly spaced, thicker sandwich-like structures along the processes. Double labeling with syntaxin-4 and calbindin antibodies, a horizontal cell marker, demonstrated syntaxin-4 localization to horizontal cell processes; whereas, double labeling with PKC antibodies, a rod bipolar cell (RBC) marker, showed a lack of co-localization, with syntaxin-4 immunolabeling occurring just distal to RBC dendritic tips. Syntaxin-4 immunolabeling occurred within VGLUT-1-immunoreactive photoreceptor terminals and underneath synaptic ribbons, labeled by CtBP2/RIBEYE antibodies, consistent with localization in invaginating horizontal cell tips at photoreceptor triad synapses. Vertical sections of retina immunostained for syntaxin-4 and peanut agglutinin (PNA) established that the prominent patches of syntaxin-4 immunoreactivity were adjacent to the base of cone pedicles. Horizontal sections through the OPL indicate a one-to-one co-localization of syntaxin-4 densities at likely all cone pedicles, with syntaxin-4 immunoreactivity interdigitating with PNA labeling. Pre-embedding immuno-electron microscopy confirmed the subcellular localization of syntaxin-4 labeling to lateral elements at both rod and cone triad synapses. Finally, co-localization with SNAP-25, a possible binding partner of syntaxin-4, indicated co-expression of these SNARE proteins in the same subcellular compartment of the horizontal cell. Taken together, the strong expression of these two SNARE proteins in the processes and endings of horizontal cells at rod and cone terminals suggests that horizontal cell axons and dendrites are likely sites of exocytotic activity.


The organization of the outer synaptic layer in the salamander retina was studied electronmicroscopically in serial sections of tissue prepared by conventional techniques or stained by the method of Golgi. Rod cell pedicles make ribbon junctions on cone cell processes, and rod cell processes invaginate cone pedicles without otherwise making any specialized contact with them. Horizontal cells make ribbon and distal junctions with the photoreceptor cell pedicles; a single horizontal cell may contact both rods and cones. Bipolar cells were observed to make either ribbon or basal junctions with the photoreceptor cell pedicles; in addition, certain processes believed to belong to bipolar cells make both ribbon and basal junctions with the same or different pedicles. A single bipolar cell may make contact with both rods and cones. Horizontal cells synapse on bipolar cell dendrites and on certain unidentified processes which in turn are also presynaptic to bipolar cells. Ascending branches of these processes invaginate deeply the rod and cone pedicles without otherwise engaging them in any junction. Horizontal cell processes are linked by two kinds of junctions: close membrane appositions, and contacts analogous to the distal junctions between horizontal cells and rod pedicles.


The synaptic contacts in the inner and outer plexiform layers of the frog retina have been identified and studied by electron microscopy. In the inner plexiform layer, two types of synaptic contact were recognized. One type, believed to be the synaptic contact of the bipolar terminals, is characterized by a synaptic ribbon in the presynaptic cytoplasm. At such ribbon contacts, there are ordinarily two postsynaptic elements, both of which usually contain numerous synaptic vesicles and appear morphologically identical. The second type of synaptic contact in the inner plexiform layer has a more conventional morpho­logy and is observed very much more frequently than are the ribbon contacts. It is characterized by a dense aggregation of synaptic vesicles clustered close to the presynaptic membrane and is thought to be the synaptic contact of the amacrine processes. The conventional synapses are presynaptic to ribbon-containing processes, ganglion cell dendrites, and other amacrine cell processes. Reciprocal contacts between processes making ribbon synapses, and processes making conventional synapses are often observed. Serial synapses between morphologically identical processes, presumably amacrine processes, are frequently seen; and up to four synapses in series between five adjacent processes have been observed. These findings suggest that in the inner plexiform layer of the frog: (1) bipolar terminals synapse primarily with amacrine processes; (2) amacrine processes synapse extensively with the processes of other amacrine cells; and (3) ganglion cells are driven primarily by the amacrine cells. In the outer plexiform layer, processes penetrate into invaginations in the bases of the receptor terminals and lie in close proximity to the synaptic ribbons of the terminals, where the processes presumably receive synaptic input from the receptors. Elsewhere in the outer plexiform layer, knob-like processes, probably from horizontal cells, make conventional synaptic contacts with other horizontal cell processes and probably with bipolar dendrites.


1985 ◽  
Vol 53 (3) ◽  
pp. 699-713 ◽  
Author(s):  
S. A. Bloomfield ◽  
J. E. Dowling

Intracellular recordings were obtained from horizontal and bipolar cells of the superfused, isolated retina-eyecup of the rabbit. The putative neurotransmitters aspartate, glutamate, and several analogues were added to the superfusate while the membrane potential and light-responsiveness of the retinal neurons were monitored. Both L-aspartate and L-glutamate mimicked the actions of the endogenous photoreceptor transmitter on horizontal cells, on-bipolar cells, and off-bipolar cells. At applied concentrations of 2.5-20 mM, the actions of L-aspartate and L-glutamate were indistinguishable. D-aspartate potentiated the effects of both L-aspartate and L-glutamate on horizontal cells. This suggests that active uptake systems for these amino acids exist in the outer plexiform layer (OPL) of the rabbit retina. The glutamate analogue kainate produced effects similar to those of aspartate and glutamate on second-order neurons, but at concentrations lower by over two orders of magnitude. The glutamate analogue quisqualate had effects similar to kainate but with much less potency. The aspartate analogue n-methyl DL-aspartate (NMDLA) antagonized the effects of the photoreceptor transmitter on horizontal and off-bipolar cells. This action of NMDLA was only observed at low concentrations (50 microM). In addition, NMDLA could block the effects of exogenously applied kainate. The NMDLA had no clear effects on on-bipolar cells. The glutamate analogue 2-amino-4-phosphonobutyrate reversibly blocked the responses of on-bipolar cells but had no effect on either horizontal or off-bipolar cell responses. This suggests that on-bipolar cells possess a unique synaptic receptor. The aspartate analogue 2-amino-3-phosphonoproprionate did not show this selectivity, suggesting that this unique receptor is a glutamate-preferring receptor. The antagonists alpha-methyl glutamate, alpha-amino adipate, and glutamate diethyl ester all showed only a weak ability to antagonize the actions of the photoreceptor transmitter on second-order neurons. The results of this study indicate that glutamate or a glutamate-like substance is the likely transmitter of rods and cones in the rabbit retina. A comparison of the present findings with those previously obtained in lower vertebrate retinas suggests that the basic pharmacological design of the OPL of all vertebrate retinas is very similar.


1976 ◽  
Vol 67 (6) ◽  
pp. 639-659 ◽  
Author(s):  
R F Miller ◽  
R F Dacheux

Intracellular recordings from receptors, horizontal cells, bipolars, and amacrines have been carried out in the perfused mudpuppy eyecup. The introduction of a chloride-free (c-f) medium results in initial transient potential changes in many cells followed by a slow loss of light-evoked activity of the depolarizing bipolar, the horizontal cell, and the on depolarization of amacrine cells. The hyperpolarizing bipolar remains responsive to light stimulation in a c-f medium, but the antagonistic surround mechanism is abolished. These effects are reversible after returning to a normal ionic medium. The results of this study provide insight into the retinal connections which underlie ganglion cell receptive field organization. It is concluded that the depolarizing bipolar is excitatory to on ganglion cells and is also the pathway for on-excitation of on-off cells. The hyperpolarizing bipolar mediates the off discharge of off and on-off cells. Amacrine cells receive input from both depolarizing and hyperpolarizing bipolar cells. These findings raise the possibility that transmembrane movements of chloride ions are critical for the light responsiveness of horizontal and depolarizing bipolar cell activity.


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.


2019 ◽  
Author(s):  
Christian Behrens ◽  
Yue Zhang ◽  
Shubhash Chandra Yadav ◽  
Silke Haverkamp ◽  
Stephan Irsen ◽  
...  

AbstractIn the outer plexiform layer (OPL) of the mouse retina, two types of cone photoreceptors (cones) provide input to more than a dozen types of cone bipolar cells (CBCs). This transmission is modulated by a single horizontal cell (HC) type, the only interneuron in the outer retina. Horizontal cells form feedback synapses with cones and feedforward synapses with CBCs. However, the exact computational role of HCs is still debated. Along with performing global signaling within their laterally coupled network, HCs also provide local, cone-specific feedback. Specifically, it has not been clear which synaptic structures HCs use to provide local feedback to cones and global forward signaling to CBCs.Here, we reconstructed in a serial block-face electron microscopy volume the dendritic trees of five HCs as well as cone axon terminals and CBC dendrites to quantitatively analyze their connectivity. In addition to the fine HC dendritic tips invaginating cone axon terminals, we also identified “bulbs”, short segments of increased dendritic diameter on the primary dendrites of HCs. These bulbs are located well below the cone axon terminal base and make contact to other cells mostly identified as other HCs or CBCs. Using immunolabeling we show that HC bulbs express vesicular gamma-aminobutyric acid transporters and co-localize with GABA receptor γ2 subunits. Together, this suggests the existence of two synaptic strata in the mouse OPL, spatially separating cone-specific feedback and feedforward signaling to CBCs. A biophysics-based computational model of a HC dendritic branch supports the hypothesis that the spatial arrangement of synaptic contacts allows simultaneous local feedback and global feedforward signaling.


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