Roles of amacrine cells

[General characteristics] [Amacrine cell circuitry as revealed by EM]
[A2] [AII] [A8] [A13] [A17] [A19 and A20] [A22] [A18] [Starburst cell] [DAPI-3 cells] [Midget system amacrine cell] [References]

10. A18: the dopaminergic amacrine cell .

Fig. 30. Dopaminergic amacrine cell in cat
(59 K jpeg image)

Fig. 31. Dopaminergic and AII cells
(59 K jpeg image)

The dopaminergic amacrine cell types have been revealed by immunostaining with an antibody directed against tyrosine hydroxylase (TOH)(the rate limiting enzyme for dopamine), is a wide-field cell that stratifies almost exclusively in stratum 1 of the IPL (under the amacrine cell bodies). It has been identified with A18 cells or Type 1CA (CA=catecholamine) of the Golgi studies (Kolb et al., 1981, 1992; Mariani, 1990). Their dendrites form a densely packed network of processes leaving only few "rings" for other amacrine cell bodies and major dendrites to pass through. The rings are are beaded dendrites that appear to be synaptic points on amacrine cells, particularly the AII amacrine cell of the rod system (see above). Another feature of dopamine cells is only seen after dye injection (Dacey, 1990) or immunostaining (Kolb et al., 1990) and this that their dendrites emit long axon-like processes running in different strata of the IPL, in the ganglion cell layer and sometimes into the outer plexiform layer (OPL).

A second type of dopaminergic cell has been described in the monkey and human retinas (Hokoc and Mariani, 1987; Crooks and Kolb, 1992). This Type 2 CA cell is described as a "wispy" cell in Golgi studies (Mariani, 1990).

Fig. 32. Types of dopaminergic cells (59 K jpeg image)

There is still not a convincing electrophysiological study of the dopamine cell in the mammalian retina. However, in turtle and fish retinas the equivalent to type 1 CA cells is an ON-center cell. In turtle the cell gives a slight ON transient which continues as a sustained depolarization during the light on. At light off, it has a very distinct slow sustained hyperpolarization that lasts for several seconds. The increasing spot sizes bring out the depolarizing ON-plateau while with an annulus, a sustained OFF-surround is evident (see Fig. 33A) (Ammermüller and Kolb, 1995).

Fig. 33a. Light responses of the dopaminergic amacrine cell in the turtle retina (Ammermuller and Kolb et al. 1995) (59 K jpeg image)

Fig. 33b. Wiring diagram of the A18 amacrine cell (78 K jpeg image)

Synaptic relations of Type 1 CA cells have bee studied by electron microscopy. This amacrine makes most of its synaptic arrangements in stratum 1 of the IPL as would be predicted from its branching pattern. Sparse cone bipolar input occurs to the cell's primary dendrites in stratum 1. The cone bipolar input is either from a diffuse cone bipolar that has axons in startum 1 or else from a giant bistratified cone bipolar cells known to be present in cat and monkey retinas. Both bipolar types are probably hyperpolarizing (OFF-center) in response. Thus the fact that the dopamine amacrine cell is a depolarizing ON center cell makes the OFF center bipolar input difficult tounderstand. Both the cell body and primary dendrites in stratum 1 of the IPL also receive GABAergic and glycinergic amacrine cell inputs. Therefore it has been suggested (Critz and Marc, 1992) that the GABAergic amacrine input comes from a GABAergic amacrine intermediary between the OFF center bipolar and the dopamine cell, thereby giving the dopamine cell its ON center response (Fig. 33b). The major output of the A18 cell is in the fine network of dendrites and axon terminals surrounding the cell bodies and apical dendrites of AII and A8 cells (Kolb et al., 1991). The rings of dopamine processes srround many unfilled stained cell bodies in figure 31. So we also think it probable that the dopamine cell in the mammal makes ring contacts upon both A17 and A13 cell bodies and main dendrites in stratum 1 of the IPL (Fig. 33b). Dopamine cell axons also contact AII dendrites in sublamina b of the IPL and the few processes that run into the OPL make synapses upon the GABAergic interplexiform cell (Kolb et al., 1991). (Fig. 33b).

Dopamine cells in the fish retina are true interplexiform cells (IPC) and have profuse arborations in the inner nuclear layer and very extensive synapses upon the 3 types of horizontal cells. In the inner plexiform layer the dopamine IPC makes some synaptic connections with the Mb (rod-dominated) bipolar axon terminals (Yazulla et al. 2001).

Fig. 34A. The dopaminergic interplexiform cell of the fish retina (59 K jpeg image)

Dopamine IPCs are thought to be influential upon the horizontal cells by decreasing their light responsiveness (Hedden and Dowling, 1978) and modulating their spatial extent by uncoupling their gap junctions (Teranishi et al., 1983). Horizontal cells in all retinas are joined by gap junctions in a strong syncytium (Kaneko, 1971; reviewed in Negishi et al., 1990). Dopamine uncouples horizontal cells from the syncytium by interacting with D1 receptors, on the horizontal cell bodies and dendrites, linked to the second messenger cyclic AMP (see Dowling, 1987 and Witkovsky and Dearry 1991 for reviews on dopamine effects in the retina). In the mammalian retina a similar but lesser amount of uncoupling of horizontal cells due to dopamine has been reported (Pflug and Nelson, 1989; Bloomfield, 1993).

Fig. 34. Effects of dopamine on AII amacrine cell coupling (59 K jpeg image)

The dopamine cell is, however, primarily an amacrine cell and not an interplexiform cell, in the mammalian retina, thus their effect on inner retina circuitry would be expected to be more pronounced than on outer retina. We known that ganglion cells have their spiking properties variously altered by dopamine and by agonists and antagonists of dopamine and D1 receptors (Ikeda et al., 1986; Jensen & Daw, 1984, 1986; Thier & Alder, 1984). These neuromodulatory effects are thought to occur via amacrine intermediaries, particularly the AII cell, or by diffusion of dopamine transmitter from a distance to ganglion cell bodies and dendrites because there are no direct contacts of dopamine amacrine cells and ganglion cell dendrites. Both D1 and D2 receptors have been seen upon some ganglion cell bodies (Dearry et al., 1991; Veruki & Wässle, 1995; Wagner et al., 1993). The second effect of dopamine in the inner retina is thought to be upon amacrine cell coupling via gap junctions, somewhat analogous to the effect upon gap junction between horizontal cells in the outer plexiform layer. Dopamine uncouples AII amacrine cells, in the mammalian retina, mediated through a D1 receptor (see above) (Hampson et al., 1992; Vaney, 1994).

11. ACh amacrines: mirror symmetric starburst cells.

Golgi studies and intracellular Lucifer yellow staining, has revealed amacrine cells that are known to use acetylcholine as a neurotransmitter (Masland and Tauchi, 1986). These cells have also been called "starburst" amacrine cells and are particularly striking in appearance in turtle, rabbit and ground squirrel retinas (Famiglietti, 1983; Tauchi and Masland, 1984; Vaney, 1990; Linberg et al., 1996; Cuenca et al., 2003).

Fig. 35. Starburst amacrine cells in rabbit retina (59 K jpeg image)

Fig. 36. Lucifer yellow labeling of a starburst amacrine cell
(59 K jpeg image)

ACh amacrines occur as two mirror symmetric pairs of cells. One type, ACh-a type, has its cell body in the amacrine cell layer and its dendrites stratify in stratum 2 of sublamina a. The other type, ACh-b type, has a cell body displaced to the ganglion cell layer and its dendrites stratify in stratum 4 of sublamina b. ACh-b cells are medium-field in size but have a tremendous overlap of their dendritic trees such that as many as 70 cells overlap a single central cell in peripheral retina (Tauchi and Masland, 1984; Vaney, 1984). ACh-a type cells have slightly larger dendritic tree sizes (13% larger) and their overlap values can reach 90 or more (Vaney, 1990a). The ACh cells in the human retina are similar to those in rabbit, but less dramatic in shape and branching pattern (see below). ACh starburst cells are particularly striking in the turtle retina where the mirror symmetric amacrines are arranged in an essentially one to one relationship. (Fig. 37b) and see movie below.

Fig. 37a. Golgi staining of ACh containing amacrine cells in human retina (59 K jpeg image)

Fig. 36. Immunioabeling of a starburst amacrine cell with ChAT in turtle whole mount retina. (947 K jpeg image)

Click here to see a rotation of the mirrow symmetric starburst cells of the turtle retina. Immunostaining to ChAT. (Courtesy Nicolas Cuenca) (4K quicktime movie).

Golgi ACh containing starburst amacrine cells of the rabbit retina have been extensively studied by electron microscopy (Famiglietti, 1991). Cone bipolar and amacrine cell inputs are distributed irregularly over the entire dendritic tree, but the proximal dendrites to the cell body, containing small spines, are particularly choice for bipolar input. A small amount of AII amacrine input may occur to the proximal dendrites of the ACh-a type cell. The varicosities on the distal dendrites (see above) are the only sites of synaptic output to ganglion cells. The postsynaptic ganglion cells for both ACh-a and ACh-b type cells, are thought to be ON-OFF directional selective bistratified ganglion cells (Amthor et al., 1984, 1989; Famiglietti, 1987, 1991; Tauchi and Masland, 1984; Vaney, 1990, 1994b). Additionally, the monostratified ON-directionally selective ganglion cell may be postsynaptic to the ACh-b type cell (Famiglietti, 1991).

Fig. 38. Intracellular recordings of ACh containing amacrine cells (59 K jpeg image)

Both mirror symmetric pairs of starburst cells of the rabbit retina have been intracellularly recorded from and dye-marked by Bloomfield (1992). The a-type of the pair is an OFF-center cell giving a transient burst of small spikes at light off while the ACh-b type is an ON-center cell (top traces, above). Both types have antagonistic surrounds, (bottom trace).

ACh amacrine cells are thus thought to be involved in the generation of directional selectivity (DS) in certain retinal ganglion cells, particularly in rabbits and turtles with visual streak topography. They may not be as well developed in form and function in foveal-based retinas such as cat and human.

Fig. 39. Wiring diagram of the two types of ACh containing amacrine cells (59 K jpeg image)

12. DAPI-3 cells in the rabbit retina.

In 1997, another bistratified medium field amacrine cell that's nucleus stained with DAPI was revealed by intracellular dye injection of Lucifer yellow. It was given the name DAPI-3 (Wright et al., 1997). Since then the DAPI-3 cell has also been revealed by the fluoresecent rhodamine probe used by MacNeil and Masland (1998) (see Fig. 4a, Roles of amacrine cells) and glycine immunoreactivity in the rabbit and groundsquirrel retinas (Zucker and Ehinger, 1998; Cuenca et al., 2002). DAPI-3 cells are medium field in size i.e. have a 100 um field diameter and a profusion of overlapping dendrites as seen in wholemount views (Fig. 40b) that prove to be the two tiers of branches of a bistratified cell (Fig. 40d). One of the tiers of dendrites in sublamina a run just below the ACh a type (starburst a type) and the other tier run in sublamina b just above the ACh b type (starburst b type) cells (Fig. 40d).

Fig. 40. A comparison between DAPI-3 cells and cholinergic ACh cells (Adapted from Zucker and Ehinger, 2001)

Fig. 41. Wiring diagram of the DAP-3 cell and its relationship to the ACh amacrine cell.

The DAPI-3 cell proves to be glycinergic and can be stained with the glycine transporter (Fig. 40c, green). It is also immunopositive for GABAA receptors (Fig. 40c, red). Thus, the cell appears to be orange in the figure (40c, red and green combine to make orange stained cells with a blue DAPI nucleus, arrows). The starburst ACh cells stains with CHAT in Fig. 40d and the overlapping dendrites of the DAPI-3 cell stained for GABAA receptors are juxtaposed to the cholinergic cell's dendrites.

Zucker and Ehinger's nice study on the DAPI-3 cells and immunostaining with the glycine and GABAA transporter/receptors allowed them to draw a summary diagram of the probably manner on which the DAPI-3 amacrine cells interact with the starburst ACh cells (Fig. 41). The DAPI-3 cell is acetylcholine receptive at nicotinic and muscarinic synapses and feeds back upon the starburst cell via a glycinergic synapse (glycine receptors have been identified on starburst cells). The DAPI-3 cell also contacts the cone bipolar cell that has input to the starburst cell. We know the starburst cell contains GABA in addition to acetylcholine and the starburst cell can presumably feed forward to the DAPI-3 cell at a GABAergic synapse with GABAA receptors on the DAPI-3 cells. The starburst cell is known to synapse upon a directionally selective ganglion cell type in rabbit retina (Fig. 41). It is not clear yet whether the DAPI-3 cell exists in other mammals that do not have a pronounced visual streak as does the rabbit.

13. Midget system amacrine cell.

The calcium binding protein calretinin is found in three types of amacrine cell in the monkey and human retinas (Kolb et al., 2002). The most numerous population are the AII amacrine cells but a small- to medium-field diffuse amacrine cell and a large-field, stratified A19 type are also calretinin-immunoreactive (IR). Of these non-AII cell types, the small diffuse (or tristratified cell type, difficult to know which) is of particular interest.

Fig. 42. : Cryostat sections of calretinin-IR monkey retina to show the different amacrine cell types that are immunoreactive. Three calretinin-IR cells are shown, of which only one has all the features of an AII amacrine cell (AII). The middle cell (A, curved arrow) has very fine, beaded dendrites running in S1, S3 and S5 (fine arrows). The third cell is difficult to identify (A).

Fig. 43. The calretinin-IR amacrine of the rod-free fovea (red cell) receives inputs from diffuse cone bipolar cells (db) and both invaginating and flat midget bipolar cells (imb and fmb) and many amacrine cells types (A arrows). It makes synapses upon ON-center midget (ON mgc) and other ON-center ganglion cells (ON GCs) in sublamina b of the IPL. OFF-center ganglion cells (OFF GC) in sublamina a could be indirectly affected by the tristrat? calretinin-IR amacrines through their reciprocal synapses to dbs or fmb bipolar cells (return arrows).

Its appearance is shown in figure 42 (A, arrow) in immunostained slice preparations. The cell has a large cell body but unlike the AII cells (Fig. 42, AII) many fine dendrites are given off the cell body instead of the typical AII thick primary dendrite. The dendrites pass down to all levels of the IPL as thin, beaded and branched processes (Fig. 42, fine arrows). This small-field diffuse calretinin-IR cell is found in high numbers in the foveal, rod-free area of the retina, and in lesser numbers in the peripheral retina. Electron microscopic examination of foveal diffuse calretinin-IR cells has shown that they get synaptic input from ON- and OFF- midget bipolar terminals, reciprocate synapses to these bipolars and have synaptic output to ON center midget ganglion cells (Fig. 43, wiring diagram). In more central to peripheral retina where rods are present, the diffuse calretinin-IR amacrines are probably also in synaptic interplay with both diffuse bipolar cells and larger parasol ganglion cells (Fig. 43). Because these calretinin-IR amacrines are found in the fovea and have particular relationships with the midget bipolar and ganglion cell systems, we have suggested that they may have a role in the antagonistic surround generation for midget ganglion cells. Moreover, they could also contribute to color opponency in these ganglion cells (Kolb et al., 2002).

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[General characteristics] [Amacrine cell circuitry as revealed by EM]
[A2] [AII] [A8] [A13] [A17] [A19 and A20] [A22] [A18] [Starburst cell] [DAPI-3 cells] [Midget system amacrine cell]