Blue-cone horizontal cells in the retinae of horses and other equidae - PubMed (original) (raw)
Blue-cone horizontal cells in the retinae of horses and other equidae
D Sandmann et al. J Neurosci. 1996.
Abstract
The morphology of horizontal cells chiefly of the horse, but also of asses, mules, and a zebra, has been examined by Lucifer yellow injections into lightly fixed retinae and by immunocytochemistry. In common with other mammals, equids have a B-type horizontal cell, i.e., a cell with dendrites synapsing with cones and possessing a single axon synapsing with rods. Most mammalian retinae have a further type of horizontal cell, the A-type, also synapsing with cones but without an axon. The second type of horizontal cell in equids also has no axon; otherwise, it is most unusual. Compared with other mammalian A-type cells, it has a vary large dendritic field, both absolutely and relative to the dendritic fields of B-type cells. The dendrites are fine and sparsely branching. Their most striking feature is that they bear a low density of irregularly spaced synaptic terminal aggregates, suggesting their cone contacts are selective. Immunolabelling of S (blue)-cones in horse retina showed that they comprise, depending on retinal location, 10-25% of the cone population. For a single horse A-type cell, it is shown that 44 of its 45 terminal aggregates are congruent with the pedicles of S-cones. Immunostaining with a calbindin antibody demonstrated that each type of horizontal cell forms an independent regular mosaic. The density ratio of B- to A-type cells varied between 5 and 10. This is the first demonstration in a mammalian retina of a horizontal cell type with a direct input exclusively from S-cones.
Figures
Fig. 9.
Analysis of horse horizontal cell mosaics.Top, Mosaic of somata in a field from superior peripheral retina. Open circles are B-type, filled circles_A-type cells. The field illustrated is 1200 × 900 μm.Bottom, Nearest-neighbor distance histograms for the B-type and A-type populations (hatched) in a larger field, including the region illustrated. The histograms are well matched by the Gaussian curves (solid) describing a regular cell distribution with the same mean soma distance and SD but not by the Poissonian curves (broken) describing the nearest-neighbor distances in a random cell distribution of the same density. The_insets give the number of cells in the sample (N), the mean distance (arrowhead in histograms), the SD, and the regularity index (r).
Fig. 1.
LY-injected B-type horizontal cells in peripheral horse retina. A, Dendritic tree in the OPL, the dendrites end in clusters of terminals (terminal aggregates). An arrow_marks the axon; the initial part bears a few terminal aggregates.B, Higher magnification showing terminal aggregates (three of them marked by arrows); each group is a cluster of the synaptic contacts with one cone. C, Three axon terminal systems injected where their processes cross.Arrows indicate where the axon thickens as it branches and begins to bear terminals. D, Higher magnification of an axon terminal branch studded with short processes that end in single terminals. Scale bar in C, 50 μm for A, 100 μm for C; scale bar in D, 20 μm for_B and D.
Fig. 4.
Drawings of LY-injected horse A- and B-type horizontal cells. All dendritic trees are at the same magnification, upper scale bar. The axon terminal system (ATS) is at lower magnification, lower scale bar. Axons are marked by_arrowheads_. All cells are from superior periphery, except for the lower left B-type cell, which is from inferior periphery.
Fig. 2.
Axonal features of horse B-type cells.A, Several straight axons simultaneously filled by a single injection of LY. The axons are of a length that some of the parent cells are outside the field; four cell bodies and dendrites of B-type cells are in view. B, B-type cells labeled through their axons by DiI applied outside the field. All axons are straight, long, and originate from cells with B-type morphology. Scale bars, 100 μm.
Fig. 6.
Mule B-type horizontal cell showing S-cone contacts. The LY-injected cell was DAB-labeled with an LY antibody, and the S-cones were simultaneously stained with JH 455. The focal series shows the labeled S-cone somata (A) and their labeled axons (B) in the outer nuclear layer and in the OPL (C, D), where they reach the terminal aggregates on the B-type dendrites. Arrowheads indicate five S-cones throughout the series. Scale bar, 25 μm.
Fig. 3.
LY-injected A-type cells from peripheral horse retina. A, Low-power view of a large, sparsely branched A-type cell (arrowhead) injected in conjunction with a B-type cell. Dendrites of both cells branch in the same plane.B–D, Higher magnification of portions of A-type dendrites to show the wide-spacing of the terminal aggregates (arrows). Compare the terminal aggregate spacing with that of a B-type cell (Fig. 1_B_). Scale bars: A, 100 μm; B–D, 20 μm.
Fig. 5.
Cone photoreceptor populations in peripheral horse retina. A, B, Double immunofluorescence with M/L-cone antiserum JH 492 and S-cone antibody OS-2. A, M/L-cone outer segments visualized with Texas red. The M/L-cones have a rather high density. There are some irregular spaces. B, Same field as A showing S-cone outer segments visualized with FITC. The S-cones have a low density and are irregularly distributed. They occupy the spaces in the M/L-cone mosaic. The position of a group of five S-cones in (B) is shown by five_open circles_ in A. S-cone outer segments are larger than those of M/L-cones. In this field, the total cone density is 7500/mm2, of which S-cones are 20%.C, S-cone pattern in another retina stained by antiserum JH 455 and visualized with DAB. This antiserum also labels the inner segments and somata of S-cones. The Nomarski optics, in addition, reveals the unstained M/L-cones and the thinner, more numerous rods. Scale bar, 50 μm.
Fig. 7.
Drawings of LY-injected horse B- and A-type horizontal cells and their overlying cone mosaics. A, Cell type B with its terminal aggregates; axon arrowed.B, The circles represent the entire overlying cone mosaic as seen with Nomarski optics. The dendritic field of the B-type cell is circumscribed by a broken line. Filled circles indicate cones congruent with the cell’s terminal aggregates; open circles are cones not in contact with this particular B-type cell. Two stars mark the positions of two terminal aggregates on the cell that could not be matched to a cone.C, Cell type A with its terminal aggregates. D, Same cell as in C with addition of the overlying S-cone mosaic as determined by antiserum labeling. _Filled circles_indicate S-cones whose pedicles are congruent each with one terminal aggregate of the cell; open circles are S-cones not in contact with the cell. The arrow marks the only terminal aggregate with no matching S-cone.
Fig. 8.
Calbindin-immunostained horse horizontal cells.A, Field of peripheral retina where the DAB reaction product was intensified with nitro blue tetrazolium, showing the somata and dense dendritic plexus in the OPL formed by the B- and A-type cells (two of the five A-type cells in the field are marked by_arrows_). B, Similar field at higher power. Here the unintensified DAB reaction shows the A-type cell more intensely labeled than the B-type cells and reveals more of its sparse dendritic branching. C, LY injection of one A-type cell (arrowed) and two B-type cells. D, Same field counterstained with calbindin to show the A- and B-type cells are part of the calbindin-labeled population. Scale bars, 50 μm.
Fig. 10.
Topography of horse horizontal cells. Density distribution of A- and B-type cells (middle) and corresponding B/A density ratios (bottom) along a superior–inferior transect in nasal retina, marked as a _solid_line in the schematic retina (top). In the retinal scheme, the visual streak (dotted line), the central area (star), and the optic nerve head (open profile) are also indicated. S, Superior; I, inferior;T, temporal; N, nasal.
Fig. 11.
Horse retina. A, Flat view of the OPL stained with N52 to show the neurofilament-containing B-type cell somata and dendrites. B, Flat view of the OPL stained with a neurofibrillar method to show the dense plexus of B-type cell axons. The plexus makes the faintly stained B-type somata difficult to see. Scale bar, 100 μm.
References
- Ahnelt P, Kolb H. Horizontal cells and cone photoreceptors in primate retina: a Golgi-light microscopic study of spectral connectivity. J Comp Neurol. 1994a;343:387–405. -PubMed
- Ahnelt P, Kolb H. Horizontal cells and cone photoreceptors in human retina: a Golgi-electron microscopic study of spectral connectivity. J Comp Neurol. 1994b;343:406–427. -PubMed
- Bowmaker JK. The visual pigments of fish. Prog Ret Eye Res. 1995;15:1–31.
- Boycott BB, Dowling JE. Organization of the primate retina: light microscopy. Philos Trans R Soc Lond Biol. 1969;255:109–184. -PubMed
- Boycott BB, Peichl L, Wässle H. Morphological types of horizontal cell in the retina of the domestic cat. Proc R Soc Lond [Biol] 1978;203:229–245. -PubMed
MeSH terms
LinkOut - more resources
Full Text Sources