Outer plexiform layer
[Techniques] [Bipolar cells] [Horizontal cells] [ON and OFF center pathways] [References]
A certain degree of integration of the visual message goes on at the first synapse in the retina, in the outer plexiform layer. Here cone pedicles and rod spherules are synaptic upon various bipolar cell and horizontal cell types. In addition, as mentioned in the previous section, cone pedicles pass electrical messages between each other and between rod spherules so that a small amount of rod and cone signal mixing occurs at this layer (Kolb, 1977; Nelson, 1977).
Two important synaptic interactions that occur at the outer plexiform layer are:
The first pathways are known as the basis of successive contrast or ON and OFF pathways respectively while the second puts light and dark boundaries in simultaneous contrast and forms a receptive field structure with a center contrasted to an inhibitory surround. We shall see how these two necessary visual information processes are created by synaptic interactions at the outer plexiform layer in this chapter.
1. Techniques that have been used to understand neural pathways in the retina.
The morphologies of individual neurons that make up the retina and contribute processes for synaptic interaction in the plexiform layers have been described over the years from using various anatomical techniques. Principal amongst these is a specific neural stain named after a famous early Italian neuroanatomist, Camillo Golgi (1885), who lived at the end of the last century. This staining method was used most extensively and with extraordinary success by the great Spanish anatomist Ramon y Cajal (1892).
Fig. 1. Picture of Cajal (59 K jpeg image)
It is, in fact, the monumental studies of Ramon y Cajal that form the basis of neuroanatomy for the vertebrate nervous system in general and the retina in particular. One of Cajal's drawings of nerve cells in the retina stained by Golgi techniques is shown below.
Fig. 2. Cajal's drawing (59 K jpeg image)
Stephen Polyak, was the man most responsible for applying the Golgi stain to monkeys and chimpanzees, authoring landmark books concerning the organization of the primate retina and visual system in 1941. More contemporaneously, we continue to use the Golgi method in research on cat, monkey and human retinas (Boycott and Dowling, 1969; Kolb, 1970; Mariani, 1984a,b; Kolb, et al., 1981, 1992). Some of the cells we have described since Cajal and Polyak are shown below.
In this one figure from Cajal's book on the vertebrate retina we see photoreceptors, bipolar cells, horizontal cells and some amacrine cells types. Cajal pointed out that photoreceptors-bipolar cells-ganglion cells were involved in passing rod or cone information through the vertical pathways and that horizontal and amacrine cells were involved in lateral interactions. He introduced the idea that synaptic connections were set up between specific cell types in the plexiform layers by virtue of nerve cells' dendrites and axons costratifying precisely to ensure that the correct presynaptic cell talked to the correct postsynaptic cell.
Fig. 3. Golgi-stained neurons of cat retina (59 K jpeg image)
It becomes immediately obvious that our drawings of Golgi stained cells differ from those of Cajal, in that we have drawn complete cells from a surface or wholemount view looking into the retina mounted flat. Being able to prepare wholemounts of retinas was a great advance for our understanding of the morphologies of nerve cells in the retina for it allowed us to see complete dendritic tree spreads of stained cell, which were often truncated in the sectioned retinas that Cajal and Polyak studied. Thus we have been able to add significant numbers of new cell types to the original descriptions. Also, with the advent of electron microscopy, histochemical and immunocytochemical staining and electrophysiological single cell recording and staining, we can now direct these techniques at elucidating neural circuits in the retina in a way not available to our predecessors. All the descriptions of cells and circuits that follow in this chapter come from experiments over the years using a combination of these techniques but always with the morphological data from Golgi staining as a basis.
2. Bipolar cells.
In human retina eleven different bipolar cell types are revealed by Golgi staining (Boycott and Wassle, 1991; Kolb et al., 1992; Mariani, 1984, 1985). Ten are for cones and one type is for rods.
Fig. 4. Bipolar cell types in human retina (59 K jpeg image)
Human retina like most mammalian retinas is rod dominated outside of the fovea. Therefore rod bipolar cells form the numerically superior part of the bipolar population in human retinas.
The rod bipolar is typically a stout bipolar with a cell body situated middle to high in the inner nuclear layer and producing a tuft of dendrites entering the OPL and reaching up to different levels between cone pedicles to reach the stacked rod spherules.
 Fig. 5. Rod bipolar cell at low magnification (59 K jpeg image) |
 Fig. 6. Rod bipolar dendritic terminal (59 K jpeg image) |
The rod bipolar dendritic terminals end one to a rod spherule as the central invaginating dendrite (shown by electron microscopy above) (Kolb, 1970). In central retina rod bipolar dendritic trees are small (15 µm across) and 15-20 rods are contacted. In peripheral retina the dendritic tree is 30 µm across and contacts 40-50 rods.
Ten different types of cone bipolar are present in human retina. Seven of them are concerned with converging information from many cones. They are known as diffuse cone bipolar types (DBs). Three cone bipolar types are concerned only with single cone contacts in a one-to one relationship. These are known as midget bipolars and blue cone specific types (FMB, IMB and BB).
Some of the diffuse cone bipolars are very wide field (giant) in dendritic spread (70-100 µm) and connect with as many as 15-20 cones (Mariani, 1984a). Little is known concerning the wide-field cells and and their role in retinal processing. These cells are badly in need of further exploration. Commonly the smaller diffuse bipolar cells collect information from 5-7 cones in central retina, and 12-14 cones in peripheral retina. The midget bipolar cells contact single cones but there are two different varieties of them per cone. Thus, cones of the fovea have output to two midget bipolar cells and of course, still some output to the diffuse bipolar cells too. The two types of midget bipolar differ in their contact with the cone pedicle.
Fig. 7. Midget bipolar cell contacts (59 K jpeg image)
The invaginating midget bipolar type (IMB) connects with the cone pedicle as central invaginating dendrites (red profiles) at ribbon synapses in the cone pedicles as shown above (Kolb, 1970). Flat midget bipolar cells (FMB) contact the cone pedicle by means of semi-invaginating, wide-cleft basal junctions (green profiles) as shown above. Often FMB dendrites make two contacts with the cone pedicle on either side of the central invaginating dendrite from the other midget bipolar cell (Kolb, 1970).
A cone bipolar cell that is thought to be specific for the short wavelength cones or blue cones (S-cones) has been described in monkey (Mariani, 1984b; Kouyama and Marshak, 1990) and in human retina (Kolb et al., 1992). This blue S-cone bipolar (see below) typically contacts one cone heavily, by several dendrites converging on that particular cone pedicle as central elements at the ribbons: so it is essentially another type of midget bipolar cell, but it differs from regular IMBs and FMBs, in having also two or more wispy dendrites contacting either another cone pedicle or ending blindly in the OPL (see later chapter on S-cone pathways). There is also a giant bistratified cone bipolar cell type in primate retina (Fig. 8, GBB) that has been proposed to be involved in the blue cone system because its axonal branching level in the IPL corresponds exactly to the dendritic branching levels of the bistratified blue/yellow ganglion cell of the S-cone pathways through the retina (see later chapter on S-cone pathways) (Kolb et al., 1997).
Fig. 8. S-cone bipolar cell types of primate retina (59 K jpeg image)
The remaining diffuse bipolar types in primate retinas (Fig. 4) are analogous to cone bipolar cells of other mammalian retinas in contacting clusters of cone pedicles as mentioned above. Like the midget bipolar cells, though, these diffuse types also differ in their types of synaptic contacts with cone pedicles, being either flat contacting types (making basal junctions with cone pedicles) or invaginating and ribbon contacting types or even being types that mix these types of contacts (Hopkins and Boycott, 1995) (see also Kolb and Nelson, 1995, for a review on photoreceptor to bipolar contacts in the vertebrate retina).
[Techniques] [Bipolar cells] [Horizontal cells] [ON and OFF center pathways] [References]
Updated: June, 2001