Horizontal cell morphology in nocturnal and diurnal primates: A comparison between owl-monkey (Aotus) and capuchin monkey (Cebus)

Horizontal cell morphology was studied in the retina of the nocturnal owl-monkey,Aotus, and compared with that of its diurnal, close relative, the capuchin monkey,Cebus. Cells were initially labeled with DiI and the staining was later photoconverted in a stable precipitated using DAB as chromogen. The sizes of cell bodies, dendritic fields, and axon terminals, number of dendritic clusters, intercluster spacing, and intercone spacing were measured at increasing eccentricities. Two distinct morphological classes of horizontal cells were identified, which resembled those of H1 and H3 cells described in diurnal monkeys. A few examples of a third class, possibly corresponding to the H2 cells of diurnal monkeys, were labeled. Both H1 and H3 cells increased in size and had increasing numbers of dendritic clusters with eccentricity. H3 cells were larger and had a larger number of dendritic clusters than H1 cells. Owl-monkey H1 cells had larger dendritic fields than capuchin monkey H1 cells at all quadrants in the central and midperipheral retinal regions, but the difference disappeared in the far periphery. Owl-monkey and capuchin monkey H1 cells had about the same number of dendritic clusters across eccentricity. As owl-monkey H1 cells were larger than capuchin monkey H1 cells, the equal number of clusters in these two primates was due to the fact that they were more spaced in the owl-monkey cells. H1 intercluster distance closely matched intercone spacing for both the owl-monkey and capuchin monkey retinas. On the other hand, H3 intercluster distance was larger than intercone spacing in the retina of both primates. Owl-monkey H1 axon terminals had 2–3 times more knobs than capuchin monkey H1 axon terminals in spite of having about the same size and, consequently, knob density was 2–3 times higher for owl-monkey than capuchin monkey H1 axon terminals across all eccentricities. The differences observed between owl-monkey and capuchin monkey horizontal cells, regarding the morphology of their dendritic trees and axon terminals, may be related to the differences found in the cone-to-rod ratio in the retina of these two primates. They seem to represent retinal specializations to the nocturnal and diurnal life styles of the owl-monkey and capuchin monkey, respectively.

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Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina

Visual Neuroscience ◽

10.1017/s0952523800002455 ◽

1994 ◽

Vol 11 (3) ◽

pp. 549-560 ◽

Cited By ~ 48

Author(s):

Stephen L. Mills ◽

Stephen C. Massey

Keyword(s):

Lucifer Yellow ◽

Horizontal Cell ◽

Horizontal Cells ◽

Rabbit Retina ◽

Dye Coupling ◽

Cell Type ◽

Axon Terminals ◽

Visual Streak ◽

Dendritic Fields

AbstractBoth A- and B-type horizontal cells in the rabbit retina were labeled by brief in vitro incubations of the isolated retina in the blue fluorescent dye 4,6–diamino-2–phenylindole. Intracellular injection of Lucifer Yellow into the somata revealed the morphology of the individual cells. Dye-coupling with Lucifer Yellow was seen only between A-type horizontal cells. By contrast, injection of the tracer Neurobiotin showed dye-coupling between both A- and B-type horizontal cells. There also appeared to be coupling between the axon terminals of B-type horizontal cells.The extensive dye-coupling seen following injection of Neurobiotin into a single horizontal cell soma can be used to obtain population counts of each cell type. Staining of large numbers of each cell type across the retina showed that each type increased in number and declined in dendritic diameter as the visual streak was approached, such that relatively constant coverage across the retina was maintained. In the visual streak, A-type horizontal cells numbered 555 cells/mm2 and averaged 120 μm in diameter, compared to 1375 cells/mm2 and 100 μm for B-type horizontal cells. In the periphery, the A- and B-types numbered 250 cells/mm2 and 400 cells/mm2, respectively. The average diameters of the dendritic trees at these locations were 225 μm for the A-type and 175 μm for the B-type. Coverage across the retina averaged almost six for A-type horizontal cells and 8–10 for the B-type. A-type horizontal cells in the visual streak whose elliptical dendritic fields were shown by Bloomfield (1992) to correlate physiologically with orientation bias were shown to be dye-coupled to cells with symmetrical dendritic fields.

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Cone connections of the horizontal cells of the rhesus monkey’s retina

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1987.0001 ◽

1987 ◽

Vol 229 (1257) ◽

pp. 345-379 ◽

Cited By ~ 90

Keyword(s):

Gap Junctions ◽

Horizontal Cell ◽

Plexiform Layer ◽

Basic Feature ◽

Morphological Type ◽

Horizontal Cells ◽

Cell Contact ◽

H1 Cells ◽

Dendritic Fields ◽

Relative Differences

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.

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3H-adenosine uptake selectively labels rod horizontal cells in goldfish retina

Visual Neuroscience ◽

10.1017/s0952523800011342 ◽

1997 ◽

Vol 14 (2) ◽

pp. 207-212 ◽

Cited By ~ 16

Author(s):

Keith M. Studholme ◽

Stephen Yazulla

Keyword(s):

Staining Pattern ◽

Outer Nuclear Layer ◽

Horizontal Cell ◽

Horizontal Cells ◽

The Other ◽

Axon Terminals ◽

Adenosine Uptake ◽

Double Label ◽

Injection Methods ◽

Goldfish Retina

AbstractThere are four types of horizontal cell in the goldfish retina, three cone- and one rod-type. The neurotransmitter of only one type, the H1 (cone) horizontal cell, has been identified as GABA. 3H-adenosine uptake was examined as a possible marker for the other classes of horizontal cell. Isolated goldfish retinae were incubated in 3H-adenosine (10–40 μCi) in HEPES-buffered saline for 30 min, then fixed, embedded in plastic, and processed for light-microscopic autoradiography (ARG). For double-label immuno/ARG studies, l-μm-thick sections were processed for GABA postembed immunocytochemistry, then for ARG. 3H-adenosine uptake was localized to cone photoreceptors, presumed precursor cells in the proximal outer nuclear layer, and to a single, continuous row of horizontal cell bodies in the inner nuclear layer. No uptake was localized to the region of horizontal cell axon terminals. 3H-adenosine uptake did not colocalize with GABA-IR in H1 horizontal cells, but it did colocalize with adenosine deaminase immunoreactivity. It is concluded that 3H-adenosine uptake selectively labels rod horizontal cells in the goldfish retina based on position and staining pattern, which are similar to rod horizontal cells stained by Golgi or HRP injection methods. The use of 3H-adenosine uptake may provide a useful tool to study other properties of rod horizontal cells (i.e. development) as well as provide clues as to the transmitter used by these interneurons.

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Excitatory amino acid receptors of rod- and cone-driven horizontal cells in the rabbit retina

Journal of Neurophysiology ◽

10.1152/jn.1987.57.3.645 ◽

1987 ◽

Vol 57 (3) ◽

pp. 645-659 ◽

Cited By ~ 41

Author(s):

S. C. Massey ◽

R. F. Miller

Keyword(s):

Membrane Potential ◽

Amino Acid ◽

Excitatory Amino Acid ◽

Direct Action ◽

Horizontal Cell ◽

Nmda Antagonist ◽

Horizontal Cells ◽

Rabbit Retina ◽

Light Responses ◽

Axon Terminals

Intracellular recordings were obtained from horizontal cells in the superfused retina-eyecup preparation of the rabbit. Rod- and cone-dominated horizontal cells were studied using bath-applied excitatory amino acid analogues. Cone-dominated horizontal cell somas were depolarized by kainate (KA) or quisqualate (QQ) and their light responses were reduced or abolished. They were not affected by N-methyl-DL-aspartate (NMDLA) at concentrations up to 2 mM or by 2-amino-4-phosphonobutyrate (APB), a selective agonist for the ON bipolar cell. When synaptic transmission was blocked with cobalt, horizontal cell somas were hyperpolarized. Under these conditions, KA and QQ caused large depolarizations suggesting that these agents have a direct action on horizontal cell somas. Excitatory amino acid antagonists such as cis-2,3-piperidine dicarboxylic acid (PDA) and kynurenic acid (Kyn) hyperpolarized horizontal cell somas to the level of the light-driven membrane potential. These antagonists blocked both the light-driven responses and the depolarizing action of KA. The specific NMDA antagonist 2-amino-7-phosphonoheptanoate (AP-7) had no effect on the membrane potential or light-driven responses of horizontal cell somas. In contrast to a previous report, we found no evidence that low concentrations of NMDLA could hyperpolarize horizontal cells or act as a KA antagonist in the rabbit retina. Rod-dominated axon terminals were identified by waveform, threshold, and the presence of a large rod after-potential evoked by high light intensity. These cells were depolarized by KA and their light responses were attenuated. NMDLA and APB had no effect on these cells. The general antagonists, PDA and Kyn, hyperpolarized axon terminals and blocked their light-evoked responses. The specific NMDA antagonist, AP-7, had no effect on these cells. These results suggest that the synaptic receptors that mediate light input to both rod- and cone-dominated horizontal cells are kainate or quisqualate receptors. This implies that the rod and cone transmitters of the rabbit retina are similar, with the characteristics of an excitatory amino acid, such as glutamate.

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Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina

Visual Neuroscience ◽

10.1017/s0952523800009093 ◽

1996 ◽

Vol 13 (5) ◽

pp. 833-845 ◽

Cited By ~ 50

Author(s):

Ann K. Goodchild ◽

Tricia L. Chan ◽

Ulrike Grünert

Keyword(s):

Short Wavelength ◽

Horizontal Cell ◽

Macaque Monkey ◽

Horizontal Cells ◽

Carbocyanine Dye ◽

Cone Pigment ◽

H1 Cells

AbstractThis study describes the connectivity between horizontal cells and short-wavelength-sensitive (SWS) cones in macaque monkey retina. H1 and H2 horizontal cells were either labelled with the carbocyanine dye, Dil, or injected intracellularly with Neurobiotin. The retinas were then processed with an antiserum against human SWS cone pigment, which usually stained the entire SWS cone. In these double-labelled retinas, the pattern of connectivity of H1 (n = 91) and H2 (n = 7) cells with SWS cones has been determined. About 85% of the H1 cells examined do not contact SWS cones. The dendritic terminal knobs of five H1 cells that do contact SWS cones were counted. They have, at most, 3% of their dendritic terminal knobs at SWS cones. All H2 cells examined make contact with SWS cones. The dendritic terminal knobs of one H2 cell were counted; about 11% of the dendritic terminal knobs are at the SWS cone. We conclude that horizontal cells in macaque monkey retina show specific patterns of connectivity to SWS cones.

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Three types of GABA-immunoreactive cone horizontal cells in teleost retina

Visual Neuroscience ◽

10.1017/s0952523800004946 ◽

1992 ◽

Vol 8 (5) ◽

pp. 443-448 ◽

Cited By ~ 2

Author(s):

Eduarda Van Haesendonck ◽

Luc Missotten

Keyword(s):

Nearest Neighbor ◽

Horizontal Cell ◽

Cell Types ◽

Horizontal Cells ◽

Marine Teleost ◽

Endogenous Gaba ◽

Teleost Retina ◽

H1 Cells ◽

Neurotransmitter Substance ◽

Dorsal Retina

AbstractPeroxidase-anti-peroxidase immunocytochemistry, applied on serial semithin epoxy resin sections, was used to examine the localization of endogenous GABA in horizontal cells in the retina of a marine teleost, the dragonet (Callionymus lyra L.). The immunostaining shows that not only the external H1 cone horizontal cells label with antibodies against GABA, but also the H2 and H3 cone horizontal cells in the inner nuclear layer. The distribution of the H1 cells corresponds to that of the single cones. They are square-patterned and in the dorsal retina their density equals 20,000 cells/mm2. The estimated density of the immunostained H2 and the H3 cells in the dorsal retina is 9500 and 1300 cells/mm2, respectively. The H2 and H3 cells are not geometrically arranged, but nearest-neighbor analysis shows that these horizontal cell types do have a very regular disposition. We suggest that GABA is the likely neurotransmitter substance used by all cone horizontal cell types in teleost retina.

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Membrane currents of horizontal cells isolated from turtle retina

Journal of Neurophysiology ◽

10.1152/jn.1992.68.2.351 ◽

1992 ◽

Vol 68 (2) ◽

pp. 351-361 ◽

Cited By ~ 19

Author(s):

A. Golard ◽

P. Witkovsky ◽

D. Tranchina

Keyword(s):

Patch Clamp ◽

Bessel Function ◽

Cell Body ◽

Axon Terminal ◽

Horizontal Cell ◽

Membrane Currents ◽

Horizontal Cells ◽

Signal Transfer ◽

Axon Terminals ◽

Space Constant

1. Membrane currents of horizontal cells isolated from the retina of the turtle, Pseudemys, were characterized by the whole-cell patch-clamp technique. 2. Four membrane currents were identified: an anomalous rectifier blocked by barium, a transient A-current, a sustained L-type calcium current enhanced by Bay K 8644, and a fast, tetrodotoxin-sensitive sodium current. Each of these four currents was found in both horizontal cell somata and axon terminals. 3. The current-voltage relations of axon terminals and somata were similar, but, in the normal operating range of the cell (-30 to -50 mV), the mean slope resistance of the axon terminal was higher (1.38 G omega) than that of the soma (0.26 G omega). 4. Exposure to either glutamate, kainate, or quisqualate induced a sustained inward current in horizontal cell axon terminals. The reversal potential for this current was -3 mV when tested with voltage steps and +9.1 mV when measured by a voltage ramp. The same horizontal cells were insensitive to N-methyl-D-aspartate. 5. A continuum model was developed to compute the degree of signal transfer between a horizontal cell body and its axon terminal. The model consisted of a network of electrically coupled somata that communicates with a network of electrically coupled axon terminals through the connecting axons. The specific membrane resistances used for the model derived from the patch-clamp measures. 6. We computed the voltage change elicited in either the layer of somata or of axon terminals by a static light stimulus of arbitrary dimensions. The amplitude of a spot response as a function of its radius was given by the weighted sum of two Bessel functions with different space constants. 7. The computed responses of the cell body were dominated by the Bessel function with the smaller space constant, whereas those of the axon terminal depended primarily on the Bessel function with the larger space constant. 8. The model predicts that, in contrast to the findings in teleost retina, there is little signal transfer between the somata and axon terminals of horizontal cell in the turtle retina.

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Effects of long–term spectral deprivation on the morphological organization of the outer retina of the blue acara ( Aequidens pulcher )

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2000.0677 ◽

2000 ◽

Vol 355 (1401) ◽

pp. 1249-1252 ◽

Cited By ~ 19

Author(s):

H.–J. Wagner ◽

R.H.H. Kröger

Keyword(s):

Developmental Plasticity ◽

Morphological Changes ◽

Horizontal Cell ◽

Spectral Component ◽

Spectral Composition ◽

Horizontal Cells ◽

Morphological Organization ◽

Cone Type ◽

H1 Cells

To investigate the developmental plasticity of colour vision, we reared fish with a trichromatic cone system ( Aequidens pulcher ) under three near–monochromatic lights, differentially stimulating each spectral cone type from the larval stage to the age of at least one year. Control conditions comprised white lights of two intensities. The treatments did not affect the visual pigments, but led to significant changes in cone outer segment lengths. Furthermore, in the blue–reared group the density of single cones within the retina was reduced by two–thirds after 18 months of exposure, while no changes were observed in the other groups. The connectivity of cone horizontal cells with the single cones was influenced by the intensity and spectral composition of the rearing lights: H1 cells were more sensitive to the spectral component, whereas H2 cells responded to intensity cues. In the blue–light group the dynamics of horizontal cell synaptic spinule formation and degradation were severely compromised. These observations show that long–term spectral deprivation leads to significant morphological changes at the level of photoreceptors and horizontal cells. While the reactions of photoreceptors may be interpreted mostly in terms of compensation, the functional consequences of the changes observed on the horizontal cell level remain to be determined electrophysiologically.

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Receptor contacts of horizontal cells in the retina of the domestic cat

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1978.0104 ◽

1978 ◽

Vol 203 (1152) ◽

pp. 247-267 ◽

Cited By ~ 41

Keyword(s):

Axon Terminal ◽

Horizontal Cell ◽

Special Kind ◽

Domestic Cat ◽

Horizontal Cells ◽

Terminal System ◽

Cone Mosaic ◽

Single Axon ◽

Dendritic Fields

The terminal aggregations of A- and B-type horizontal cells, stained by the Golgi-Colonnier method, have been analysed. The pattern of the aggregations is regular and is shown to be in register with the cone mosaic. Both types of horizontal cell are in contact with at least 80% of the cones above their dendritic fields. Therefore, the different horizontal cell classes cannot be selective for a special kind of cone but must have at least 60% of the cone input in common. Each A-type horizontal cell makes contacts with between 120 and 170 cones, and each B-type horizontal cell with 60-90 cones. An individual A-type horizontal cell occupies an average of 20% of the lateral elements of the triads in a cone pedicle, but an individual B-type cell fills only some 13%. Each and every cone is connected with several of both types of horizontal cell. An estimation of the number of rods converging onto a single axon terminal system showed that it could be as many as 3000.

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