Colour receptors, and their synaptic connexions, in the retina of a cyprinid fish

Morphologically speaking, there are five kinds of cone cells in the retina of the rudd ( Scardinius erythrophthalmus ). But two of them, the principal elements of the double cones and the free principal cones, are probably functionally equivalent, while another, sparse, population of small ( oblique ) cones (which disappear in older fish), is unlikely to make a significant contribution to visual spectral sensitivity. Thus, principal and accessory cones (usually paired with one another), and single cones seem to be the three receptors which underlie the fish’s trichromacy. Photographic densitometry of individual cone cells was used to provide evidence that accessory cones contain a green-absorbing photopigment and the single cones a blue one. Other arguments are given in support of those identifications, and they also strongly suggest that principal cones contain the red-absorbing pigment. Golgi-impregnated bipolar cells were examined electron-microscopically to determine the specific patterns of synaptic connexion they make with these different, anatomically identifiable, colour cones and with the retinal rods. Three principal arrangements were distinguished (see figure 69, page 190). (1) Rod bipolar cells comprise two distinct morphological types, both of which connect exclusively to principal (red) cones as well as to the rods within the outlines of their dendritic fields. (2) Selective cone bipolar cells, more delicate neurons with considerably wider dendritic fields, connect (according to type) to one or other of the different colour cone populations. Examples analysed were specific for the accessory (green) or for the single (blue) cones; no bipolar cells were found connected only to red cones. (3) Mixed cone bipolars have the smallest dendritic fields, and connect to combinations of cones (for example, red and green, or green and blue, but not red and blue). They also have synaptic input (usually relatively sparse) from the rods. Cells were encountered connecting to all three cone types, but they were only partially analysed, and are not described at length. The light microscopic morphology of these bipolar cell types consistently reflects the detailed pattern of connexion each makes with the different receptor populations (just as the morphology of the cones reflects the spectral properties of their photopigment). But while their synaptic connectivity is generally highly specific for cone type, they do occasionally make anomalous connexions with the ‘wrong’ receptors. There is a high degree of divergence (page 85) at the receptor-bipolar synapses, and the different kinds of cones each characteristically connect to different numbers of bipolar cells. Principal (red) cones, which are the most numerous, individually connect to more bipolars than cones of other types, whose characteristic synaptic divergence is likewise related to the frequency with which they occur in the retina. However, rods, which are much more numerous than cones, do not conform with this generalization. The selectivity with which the synaptic terminals of the different cones are connected together by their invaginating basal processes was also examined. These processes link neighbouring synaptic terminals of differently coloured cones: specifically, principal (red) cone basal processes invaginate accessory (green) cone pedicles, and vice versa. Single (blue) cone basal processes connect only to accessory cone pedicles, but that synaptic relation is not reciprocated. These synapses between the cones have important bearing upon interpretation of the bipolar cell connectivity patterns. In their light, the interaction between colour channels which the convergence of different cones onto the mixed cone bipolar dendrites mediates, seems to re-iterate a process already undertaken more peripherally. Likewise, whereas the anatomy of the selective cone bipolars appears designed to convey activity from the individual cone populations, the responses of the receptors they sample must already be influenced by activity in other colour channels.

2010 ◽  
Vol 28 (1) ◽  
pp. 29-37 ◽  
Author(s):  
HANNAH R. JOO ◽  
BETH B. PETERSON ◽  
TONI J. HAUN ◽  
DENNIS M. DACEY

AbstractParallel processing of visual information begins at the first synapse in the retina between the photoreceptors and bipolar cells. Ten bipolar cell types have been previously described in the primate retina: one rod and nine cone bipolar types. In this paper, we describe an 11th type of bipolar cell identified in Golgi-stained macaque retinal whole mount and vertical section. Axonal stratification depth, in addition to dendritic and axonal morphology, distinguished the “giant” cell from all previously well-recognized bipolar cell types. The giant bipolar cell had a very large and sparsely branched dendritic tree and a relatively large axonal arbor that costratified with the DB4 bipolar cell near the center of the inner plexiform layer. The sparseness of the giant bipolar’s dendritic arbor indicates that, like the blue cone bipolar, it does not contact all the cones in its dendritic field. Giant cells contacting the same cones as midget bipolar cells, which are known to contact single long-wavelength (L) or medium-wavelength (M) cones, demonstrate that the giant cell does not exclusively contact short-wavelength (S) cones and, therefore, is not a variant of the previously described blue cone bipolar. This conclusion is further supported by measurement of the cone contact spacing for the giant bipolar. The giant cell contacts an average of about half the cones in its dendritic field (mean ± s.d. = 52 ± 17.6%; n = 6), with a range of 27–82%. The dendrites from single or neighboring giant cells that converge onto the same cones suggest that the giant cell may selectively target a subset of cones with a highly variable local density, such as the L or M cones.


2010 ◽  
Vol 28 (1) ◽  
pp. 77-93 ◽  
Author(s):  
V.P. CONNAUGHTON

AbstractZebrafish are an existing model for genetic and developmental studies due to their rapid external development and transparent embryos, which allow easy manipulation and observation of early developmental stages. The application of the zebrafish model to vision research has allowed for examination of retinal development and the characteristics of different retinal cell types, including bipolar cells. In particular, bipolar cell development, including differentiation, maturation, and gene expression, has been documented, as has physiological properties, such as voltage- and ligand-gated currents, and neurotransmitter receptor and ion channel expression. Mutant strains and transgenic lines have been used to document how bipolar cell connections and/or development may be altered, and toxicological studies examining how environmental factors may impact bipolar cell activity have been performed. The purpose of this paper was to review the existing literature on zebrafish bipolar cells, to provide a comprehensive overview of current information pertaining to this retinal cell type.


2018 ◽  
Author(s):  
Marion F. Haug ◽  
Manuela Berger ◽  
Matthias Gesemann ◽  
Stephan C. F. Neuhauss

AbstractThe retina is a complex neural circuit in which visual information is transmitted and processed from light perceiving photoreceptors to projecting retinal ganglion cells. Much of the computational power of the retina rests on signal integrating interneurons, such as bipolar cells in the outer retina. While mammals possess about 10 different bipolar cell types, zebrafish (Danio rerio) has at least six ON-type, seven OFF-type, and four mixed-input bipolar cells. Commercially available antibodies against bovine and human conventional protein kinase C (PKC) α and -β are frequently used as markers for retinal ON-bipolar cells in different species, despite the fact that it is not known which bipolar cell subtype(s) they actually label.Moreover, the expression pattern of the five prkc genes (coding for PKC proteins) has not been systematically determined. While prkcg is not expressed in retinal tissue, the other four prkc (prkcaa, prkcab, prkcba, prkcbb) transcripts were found in different parts of the inner nuclear layer and some as well in the retinal ganglion cell layer.Immunohistochemical analysis in adult zebrafish retina using PKCα and PKCβ antibodies showed an overlapping immunolabeling of ON-bipolar cells that are most likely of the BON s6L or RRod type and of the BON s6 type. However, comparison of transcript expression with immunolabling, implies that these antibodies are not specific for one single zebrafish conventional PKC, but rather detect a combination of PKC -α and -β variants.


Cells ◽  
2022 ◽  
Vol 11 (1) ◽  
pp. 161
Author(s):  
Daniëlle Swinkels ◽  
Yannick Das ◽  
Sai Kocherlakota ◽  
Stefan Vinckier ◽  
Eric Wever ◽  
...  

Retinal degeneration is a common feature in peroxisomal disorders leading to blindness. Peroxisomes are present in the different cell types of the retina; however, their precise contribution to retinal integrity is still unclear. We previously showed that mice lacking the central peroxisomal β-oxidation enzyme, multifunctional protein 2 (MFP2), develop an early onset retinal decay including photoreceptor cell death. To decipher the function of peroxisomal β-oxidation in photoreceptors, we generated cell type selective Mfp2 knockout mice, using the Crx promotor targeting photoreceptors and bipolar cells. Surprisingly, Crx-Mfp2−/− mice maintained photoreceptor length and number until the age of 1 year. A negative electroretinogram was indicative of preserved photoreceptor phototransduction, but impaired downstream bipolar cell signaling from the age of 6 months. The photoreceptor ribbon synapse was affected, containing free-floating ribbons and vesicles with altered size and density. The bipolar cell interneurons sprouted into the ONL and died. Whereas docosahexaenoic acid levels were normal in the neural retina, levels of lipids containing very long chain polyunsaturated fatty acids were highly increased. Crx-Pex5−/− mice, in which all peroxisomal functions are inactivated in photoreceptors and bipolar cells, developed the same phenotype as Crx-Mfp2−/− mice. In conclusion, the early photoreceptor death in global Mfp2−/− mice is not driven cell autonomously. However, peroxisomal β-oxidation is essential for the integrity of photoreceptor ribbon synapses and of bipolar cells.


2020 ◽  
Author(s):  
Amanda J. McLaughlin ◽  
Kumiko A. Percival ◽  
Jacqueline Gayet-Primo ◽  
Teresa Puthussery

AbstractAdapting between scotopic and photopic illumination involves switching the routing of retinal signals between rod and cone-dominated circuits. In the daytime, cone signals pass through parallel On and Off cone bipolar cells, that are sensitive to increments and decrements in luminance, respectively. At night, rod signals are routed into these cone-pathways via a key glycinergic interneuron, the AII amacrine cell (AII-AC). In primates, it is not known whether AII-ACs contact all Off-bipolar cell types indiscriminately, or whether their outputs are biased towards specific Off-bipolar cell types. Here, we show that the rod-driven glycinergic output of AII-ACs is strongly biased towards a subset of macaque Off-cone bipolar cells. The Off-bipolar types that receive this glycinergic input have sustained physiological properties and include the Off-midget bipolar cells, which provide excitatory input to the Off-midget ganglion cells (parvocellular pathway). The kinetics of the glycinergic events are consistent with the involvement of the α1 glycine receptor subunit. Taken together with results in mouse retina, our findings point towards a conserved motif whereby rod signals are preferentially routed into sustained Off signaling pathways.Significance StatementVisual signals pass through different retinal neurons depending on the prevailing level of illumination. Under night-time light levels, signals from rods pass through the AII amacrine cell, an inhibitory interneuron that routes rod signals into On and Off bipolar cells to detect increments and decrements in light intensity, respectively. Here, we show in primate retina that the output of AII amacrine cells is strongly biased towards specific Off bipolar cell types, which suggests that rod signals reach the brain via specific neural channels. Our results further our understanding of how visual signals are routed through visual circuits during night-time vision.


1993 ◽  
Vol 10 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Ann H. Milam ◽  
Dennis M. Dacey ◽  
Alexander M. Dizhoor

AbstractHuman, macaque monkey, and rat retinas were immunostained with a polyclonal antibody preparation against purified recoverin, a 23-kD calcium-binding protein isolated from bovine retina that localizes to rods and cones (Dizhoor et al., 1991). In addition to immunoreactive photoreceptors, we have identified subpopulations of recoverin-positive bipolar cells in all three species. Results from immunostaining with progressive dilutions of anti-recoverin and preadsorption of the antibody with a dilution series of purified recoverin showed that photoreceptors and bipolar cells had similar affinities for the antibody and suggested that the molecule recognized by the antibody in both cell types is recoverin. Immunoreactivity for recoverin and protein kinase C, a selective marker for all rod bipolar cells, was found in separate bipolar cell populations. Recoverin immunoreactivity is therefore a characteristic of certain cone bipolar cell types.In rat retina, anti-recoverin labeled two morphologically distinct subpopulations of cone bipolar cells whose axonal arbors stratified at different depths in the inner plexiform layer (IPL). The bipolar cells labeled with anti-recoverin did not correspond to those that were reactive for calbindin, another cone bipolar cell marker.Human and monkey retinas also had two populations of cone bipolar cells that were recoverin-positive. One population showed a distinct pattern of narrow bistratification at the outer border of the IPL and a regular mosaic arrangement of its axonal arbors, suggesting that the entire population of a single cone bipolar type was labeled. Cell density, dendritic morphology, and axonal-field size and stratification indicate that anti-recoverin selectively stains the flat midget (presumed OFF-center) cone bipolar cell type observed previously in Golgi preparations. By contrast the second bipolar cell population had axonal stratification in the inner half of the IPL and showed an unusual but consistent morphology and spatial distribution. Individual cells were intensely stained but were present at an extremely low density (~2−5 cells/mm2). These cells had multibranched dendritic trees characteristic of the diffuse bipolar cell class, but very small axonal fields in the size range of the midget bipolar class. Neither of the two recoverin-positive bipolar cell types in monkey was labeled with anti-calbindin or anti-cholecystokinin. An antibody preparation against bovine pineal hydroxyindole-O-methyltransferase (HIOMT) labeled photoreceptors and bipolar cells that closely resembled the recoverin-positive bipolar cells in human and rat retinas. Preadsorption of this antibody preparation with purified recoverin abolished immunostaining of the bipolar cells, suggesting that the anti-HIOMT preparation contains antibodies against recoverin, which is known to be present in the bovine pineal gland.


1997 ◽  
Vol 14 (4) ◽  
pp. 789-794 ◽  
Author(s):  
Noga Vardi ◽  
Katsuko Morigiwa

AbstractThe rod bipolar cell and about five types of ON cone bipolar cells depolarize to light by employing a sign-reversing metabotropic glutamate receptor. Glutamate responses are similar in both rod bipolar and cone bipolar cells, but the receptor mediating this response (mGluRo) was so far demonstrated only in rod bipolar cells. To test if ON cone bipolar cells also express mGluR6, we immunoreacted rat retina with an antibody specific for mGluRo, and studied the staining from serial ultrathin sections. We demonstrate that mGluR6 is indeed expressed in the dendritic tips of cone bipolar cells, the majority of which receive a ribbon synapse, and thus probably are ON cone bipolar cells. We further show that half of the dendritic tips contacting the cones stain for mGluR6, thus implying that all ON cone bipolar cell types express mGluR6.


2003 ◽  
Vol 20 (6) ◽  
pp. 589-600 ◽  
Author(s):  
SILKE HAVERKAMP ◽  
FRANCOISE HAESELEER ◽  
ANITA HENDRICKSON

As more human retinas affected with genetic or immune-based diseases become available for morphological analysis, it is important to identify immunocytochemical markers for specific subtypes of retinal neurons. In this study, we have focused on bipolar cell markers in central retina. We have done single and double labeling using several antisera previously utilized in macaque monkey or human retinal studies and two new antisera (1) to correlate combinations of antisera labeling with morphological types of bipolar cells in human retina, and (2) to compare human labeling patterns with those in monkey retina. Human bipolar cells showed a wide range of labeling patterns with at least ten different bipolar cell types identified from their anatomy and marker content. Many bipolar cell bodies in the outer part of the inner nuclear layer contained combinations of protein kinase C alpha (PKCα), Islet-1, glycine, and Goα. Bipolar cells labeled with these markers had axons terminating in the inner half of the inner plexiform layer (IPL), consistent with ON bipolar cells. Bipolar cell bodies adjacent to the amacrine cells and with axons in the outer half of the IPL contained combinations of recoverin, glutamate transporter-1, and PKCβ, or CD15 and calbindin. Bipolar cells labeled with these markers were presumed OFF bipolar cells. Calcium-binding protein 5 (CaB5) labeled both putative ON and OFF bipolar cells. Using this cell labeling as a criteria, most cell bodies close to the horizontal cells were ON bipolar cells and almost all bipolar cells adjacent to the amacrine cells were OFF with a band in the middle 2–3 cell bodies thick containing intermixed ON and OFF bipolar cells. Differences were found between human and monkey bipolar cell types labeled by calbindin, CaB5, and CD15. Two new types were identified. One was morphologically similar to the DB3, but labeled for CD15 and CaB5. The other had a calbindin-labeled cell body adjacent to the horizontal cell bodies, but did not contain any accepted ON markers. These results support the use of macaque monkey retina as a model for human, but caution against the assumption that all labeling patterns are identical in the two primates.


2017 ◽  
Vol 34 ◽  
Author(s):  
PATRICK W. KEELEY ◽  
JASON J. KIM ◽  
SAMMY C.S. LEE ◽  
SILKE HAVERKAMP ◽  
BENJAMIN E. REESE

AbstractRetinal bipolar cells spread their dendritic arbors to tile the retinal surface, extending them to the tips of the dendritic fields of their homotypic neighbors, minimizing dendritic overlap. Such uniform nonredundant dendritic coverage of these populations would suggest a degree of spatial order in the properties of their somal distributions, yet few studies have examined the patterning in retinal bipolar cell mosaics. The present study examined the organization of two types of cone bipolar cells in the mouse retina, the Type 2 cells and the Type 4 cells, and compared their spatial statistical properties with those of the horizontal cells and the cholinergic amacrine cells, as well as to random simulations of cells matched in density and constrained by soma size. The Delauney tessellation of each field was computed, from which nearest neighbor distances and Voronoi domain areas were extracted, permitting a calculation of their respective regularity indexes (RIs). The spatial autocorrelation of the field was also computed, from which the effective radius and packing factor (PF) were determined. Both cone bipolar cell types were found to be less regular and less efficiently packed than either the horizontal cells or cholinergic amacrine cells. Furthermore, while the latter two cell types had RIs and PFs in excess of those for their matched random simulations, the two types of cone bipolar cells had spatial statistical properties comparable to random distributions. An analysis of single labeled cone bipolar cells revealed dendritic arbors frequently skewed to one side of the soma, as would be expected from a randomly distributed population of cells with dendrites that tile. Taken together, these results suggest that, unlike the horizontal cells or cholinergic amacrine cells which minimize proximity to one another, cone bipolar cell types are constrained only by their physical size.


1988 ◽  
Vol 91 (2) ◽  
pp. 275-287 ◽  
Author(s):  
T Saito ◽  
T Kujiraoka

ON and OFF bipolar cells were identified in the light-adapted carp retina by means of intracellular recording and Lucifer yellow dye injection. The receptive field centers, determined by measuring the response amplitudes obtained by centered spots of different diameters, were 0.3-1.0 mm for ON bipolar cells and 0.3-0.4 mm for OFF bipolar cells. These central receptive field values were much larger than the dendritic field diameters measured by histological methods. Simultaneous intracellular recordings were made from pairs of neighboring bipolar cells. Current of either polarity injected into one member of a bipolar cell pair elicited a sign-conserving, sustained potential change in the other bipolar cell. The coupling efficiency was nearly identical for both depolarizing and hyperpolarizing currents. The maximum separation of coupled bipolar cells was approximately 130 microns. This electrical coupling was reciprocal and summative, and it was observed in cell types of similar function and morphology. Dye coupling was observed in 4 out of 34 stained cells. These results strongly suggest that there is a spatial summation of signals at the level of bipolar cells, which makes their central receptive fields much larger than their dendritic fields.


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