Helga Kolb

Amacrine cells, bipolar cells and ganglion cells of the cat retina: a Golgi study.

Abstract Neuronal types contributing to the inner plexiform layer of the cat retina are described based primarily on light microscopy of Golgi-impregnated retinal whole-mounts. Cells have been characterized on morphological criteria that include dendritic branching patterns, dendritic tree sizes, cell body sizes and stratification of processes in the inner plexiform layer. Nine different types of bipolar cell, 22 different types of amacrine cell and 23 different types of ganglion cell can be distinguished using one or more of these morphological criteria. The significance of the different morphological types of cells is discussed, particularly in relationship to the functional bisublamination of the cat inner plexiform layer.

Rod and cone pathways in the inner plexiform layer of cat retina

In cat retina, rod bipolar terminials do not synapse on ganglion cells but on two types of amacrine cell (types I and II). Cone bipolars synapse directly on ganglion cells and on type I amacrines. The type II amacrine appears to play a special internuncial role between bipolars and ganglion cells in the rod system.

The inner plexiform layer in the retina of the cat: electron microscopic observations

SummaryNeural connections of cells ramifying in the inner plexiform layer of the cat retina have been studied by serial section electron microscopy. Flat cone bipolars and invaginating cone bipolars segregate their axon terminals to different sublaminae of the IPL (sublaminaa and sublaminab, respectively) where they relate to different subtypes of the same class of ganglion cell (a andb types respectively).Rod bipolar axon terminals end solely in sublaminab and synapse with amacrine cells (AI and AII). AI provides reciprocal synapses to clusters of rod bipolar axon terminals. The AII amacrine provides rod input toa type ganglion cells by means of chemical synapses and tob type ganglion cells through gap junctions with invaginating cone bipolar terminals.Amacrine cells exist which interconnect rod and cone bipolars, but some amacrines appear to be related specifically to neurons branching in particular sublaminae. Both large- and small-bodied ganglion cells have amacrine-dominated input while the medium-bodied ganglion cells with small dendritic trees have cone bipolar-dominated input.

The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations

SummaryThe outer plexiform layer of the cat retina has been examined by electron microscopy of random and serial ultrathin sections in order that neural profiles might be positively identified and their synaptic relationships studied. Photoreceptors are interconnected by means of gap junctions as are the A horizontal cells. B horizontal cells and axon terminals do not appear to be engaged in any synapses apart from those with photoreceptors, while A horizontal cells make rare ‘junctions’ with cone bipolars only. Interplexiform cell processes probably account for all the conventional chemical synapses in the outer plexiform layer of cat retina.

Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina.

After intracellular recording, bipolar cells of the cat retina have been stained with HRP and their contacts in the outer and inner plexiform layers examined by electron microscopy. Rod bipolars and cone bipolar cb6 make invaginating, ribbon related contacts with photoreceptors, hyperpolarize in response to light, and have axons terminating in layer b of the IPL. The axon terminal of cb2 ends in layer a of the IPL and its basal contacts with cones mediate hyperpolarizing light-responses. Cone bipolar cb5 is a center-depolarizing type with an axon ending in layer b but its cone contacts are at semi-invaginating basal junctions. Except for the amacrine-contacting rod bipolar cell, all cone bipolar types synapse with both amacrine and ganglion cells in the inner plexiform layer. In addition cb5 contacts AII amacrine cells with large gap junctions, and is physiologically rod dominated.

Rod pathways in the retina of the cat

Neurons involved in the transfer of rod signals to the ganglion cells in the retina of the cat have been recorded from and stained with horseradish peroxidase (HRP) and their synaptic connections determined by electron microscopy. The single morphological type of rod bipolar cell responds with a sustained hyperpolarization to light and in turn drives at least five morphologically different types of amacrine cells, each of which has a unique response pattern. Two amacrines respond with either a transient (AII) or a sustained (A17) depolarization to light, while three amacrines give transient (A8) or sustained (A6, A13) hyperpolarizations. Circuitry whereby rod signals reach both on-centre and off-centre ganglion cells is discussed.

The synaptic organization of the dopaminergic amacrine cell in the cat retina

SummaryThe dopaminergic amacrine cells of the cat retina have been stained by immunocytochemistry using an antibody to tyrosine hydroxylase (Toh). The complete population of Toh+cells has been studied by light microscopy of retinal wholemounts to evaluate morphological details of dendritic structure and branching patterns. Selected Toh+amacrine cells have been studied by serial-section electron microscopy to analyse synaptic input and output relationships. The majority of Toh+amacrine cells occur in the amacrine cell layer of the retina and have their dendrites ramifying and forming the characteristic rings in stratum 1 of the inner plexiform layer. A minority of Toh+cells have cell bodies displaced to the ganglion cell layer but their dendrites also stratify in stratum 1. All Toh+cells have some dendritic branches running in stratum 2 as well as in stratum 1, and frequently they have long ‘axon-like’ processes (500–1000 μm long) dipping down to run in stratum 5 before passing up to rejoin the major dendritic arbors in stratum 1. In addition Toh+stained processes follow blood vessels in the inner plexiform layer and in the ganglion cell layer. A population of Toh+cells found in the inferior retina appears to give rise to stained processes that pass to the outer plexiform layer and therein to run for as far as one millimeter.Electron microscopy reveals that Toh+amacrine cells are postsynaptic to amacrine cells and a few bipolar cell terminals in stratum 1 of the inner plexiform layer and are primarily presynaptic to All amacrine cell bodies and lobular appendages, and to another type of amacrine cell body and amacrine dendrites hypothesized to be the A17 amacrine cell. The Toh+dendrites in stratum 2 are presynaptic to All lobular appendages primarily. Stained ‘axon-like’ processes running in stratum 5 prove to be presynaptic to All amacrine dendrites as they approach the rod bipolar axon terminals and they may also be presynaptic to the rod bipolar terminal itself. The Toh+stained dendrites that have been followed in the outer plexiform layer run along the top of the B-type horizontal cell somata and may have small synapses upon them. The only clear synapses seen in the outer plexiform layer are from the Toh+profiles upon vesicle filled amacrine-like profiles that are in turn presynaptic to bipolar cell dendrites in the outer plexiform layer. We presume the cells postsynaptic to the Toh+dendrites in the outer plexiform layer are interplexiform cells. Finally the Toh+profiles that course along blood vessel walls and in the ganglion cell layer appear to end either against the basal lamina of the blood vessel or at intercellular channels of vesicle-laden Muller cell end-feet.

Synaptic connections of the interplexiform cell in the retina of the cat

SummaryElectron microscopy of Golgi-impregnated material and of well fixed, ultrathin serial sections has revealed the synaptic connections of interplexiform cells in cat retina. In the inner plexiform layer these cells are postsynaptic to amacrine cells and probably presynaptic to both bipolars and amacrines. In the outer plexiform layer they are presynaptic to rod and cone bipolar cells and also pre- and postsynaptic to other interplexiform cell dendrites. The interplexiform cell in cat retina appears to be concerned with feeding back information from the inner plexiform layer to the dendrites of bipolar cells in the outer plexiform layer.

Interplexiform Cells of the Mammalian Retina and their Comparison with Catecholamine-Containing Retinal Cells

Retinal interplexiform cells have processes that branch within both the inner and outer plexiform layers. Their morphology is described from Golgi-preparations of cat, rhesus macaque and squirrel monkey retinae. Comparisons are made with similar cells, known to be catecholamine-containing, which have been observed histofluorometrically in the teleost fish and New World monkeys. It is concluded that there may be more than one pharmacological type of interplexiform cell. In addition an inner nuclear layer plexus of fibres is described for the first time from Golgi-material of the squirrel monkey’s retina. Electron microscopy reveals that this plexus synapses within the inner nuclear layer on to bipolar and amacrine cells. It is compared with the catecholamine-containing inner nuclear layer plexus of New World monkeys.

Dopamine-containing amacrine cells of rhesus monkey retina parallel rods in spatial distribution

Dopamine-containing amacrine cells of rhesus monkey were found everywhere outside of the foveola in whole, flat retinas by the formaldehyde-glutaraldehyde fluorescent method. There were about 7500 such cells in a single retina and their density, determined by cell counts and measured by a nearest neighbor method, was minimal in foveal and peripheral regions and maximal at 3 mm from the center of the fovea. Compared to density distributions of other retinal neuron types, dopamine-containing amacrine cells correlated only with rods, which also had a peak density at 3 mm eccentricity. Cones and ganglion cells peaked in the foveal pit, or within 1 mm of it, respectively. As the distribution of dopamine-containing cells followed that of rods, it is suggested that dopamine could be involved in the rod neuronal circuitry of primates.