Neurotransmitters in the retina
[General characteristics]
[Glutamate]
[Gamma aminobutyric acid]
[Glycine]
[Dopamine]
[Acetylcholine]
[Serotonin]
[Adenosine]
[Substance P]
[Other neuropeptides]
[Nitric oxide]
[Amacrine cell populations]
[References]
1. General characteristics.
Todays research on the retina focuses a great deal of attention on
neurotransmission between the neurons of the retina. Varous techniques using
autoradiography, immunocytochemistry and molecular biology are being used
to mark neurons for neurochemicals, their synthesizing enzymes, calcium binding proteins and receptors and transporters
of these neurochemicals. Cells immunostained with antibodies to the various neurotransmitter candidates
give particularly spectacular images by confocal microscopy because they become stained to their
finest dendrites and so can be readily classified against their Golgi-stained
equivalents. Furthermore, the whole population of neurotransmitter specific
neurons are stained so one can understand their topographical organization into
mosaics across the entire retina. Some immunocytochemistry for the common
neurotransmitter candidates has been performed on the human retina (Davanger,
1992; Crooks and Kolb, 1992) but more has been done in the monkey retina and so
far the findings are the same in general. The consistency of cell types
staining across species boundaries, in mammals at least, suggest that most,
with a few exceptions, of the neurotransmitters, neuromodulators and
neuropeptides discovered in nonhuman retinas are present in human retina
too. 2. The neurotransmitter of neurons of the vertical pathways through the retina
is glutamate.
Glutamate is the neurotransmitter of the
neurons of the vertical pathways through the retina. All photoreceptor types,
rods and cones, use the excitatory amino acid glutamate to transmit
signals to the next order neuron in the chain (See chapter on glutamate and Massey, 1990, for review).
There was originally some evidence for the closely related amino acid,
aspartate, being present in rods but the latest sophisticated techniques of
demonstrating amino acid signatures in retinal neurons cannot confirm aspartate
as a retinal neurotransmitter at all (Marc et al., 1995).Uptake, release and
action of glutamate and agonists upon second-order neurons in slice
preparations or isolated cells in tissue culture have also all confirmed
glutamate to be the neurotransmitter acting at the first synapse in the retina
(see Lasater, 1992 for review). The action of the photoreceptor
neurotransmitter upon the second-order neurons is through two different types
of sensory channels though. The one type of postsynaptic receptor type is the
metabotropic glutamate channel (mGluR6) that involves a second messenger cascade and cyclic GMP for activation of the channel (in the ON-center bipolar cell)
whereas the other is an ionotropic channel via at least two types of AMPA receptors and Na ions
(OFF-center bipolar and horizontal cells) (Slaughter and Miller, 1981, 1983a,b;
Nawy and Jahr, 1990). Photoreceptors in most vertebrates including human, have
a content of D2 dopamine receptors somewhere upon there surface (Witkovsky and
Dearry, 1991).
Fig. 1. Distribution of Glutamate immunoreactivity in human retina (78 K jpeg image)
Glutamate is also considered to be the neurotransmitter of all bipolar cells and most ganglion cells in the vertebrate retina including the monkey retina (Marc et al., 1995; Kalloniatis and Marc, personal communication). In an immunocytochemical study of the human retina a similar conclusion was drawn by us. All the ganglion cells appeared to label strongly with antibodies to glutamate (Crooks and Kolb, 1992) (see Fig. 1, above).
Bipolar cells have receptor channels that are either of the metabotropic type, mGluR6,(APB sensitive) or ionotropic type (AMPA) at their dendrites in the OPL, while their axonal ending in the IPL have channels and receptors for GABA (A, B and C types), D1 dopamine and glycine because, of course, all kinds of amacrine cells are presynaptic at these sites in the IPL neuropil. Ganglion cells are as diverse in receptor sensors as the bipolar cells with the addition of receptors to acetylcholine (Keyser et al., 1993), and the first appearance in the retina of NMDA glutamate receptors that are typical in the brain (Massey and Miller, 1988; Yazejian and Fain et al., 1992).
Amacrine cells
Recently an amacrine cell type has also been shown to contain the glutamate transporter, vesicular glutamate transporter 3, shortened to VGLUT3 (Johnson et al, 2004; Haverkamp and Wassle, 2004). VGLUTs are used to concentrate cystolic glutamate into the synaptic vesicles. Typically in the retina the VGLUT1 isoform is expressed in photoreceptors and bipolar cells and the VGLUT2 in ganglion cells. The amacrine cell type that can be immunostained to the antibody to VGLUT3 is found to be a small-field amacrine cell with varicose processes that are restricted in branching to the OFF laminae (S1 and S2) of the IPL (Fig. 2A). It is also immunoreactive to the transmitter glycine as seen in Figures 2B and C, but not reactive for GABA, dopamine (Fig. 3A, B and C) or acetylcholine. Figures 3A, B, and C show that the dopamine cell and its dendrites run above the branches of the VGLUT3 cell and indeed appear to be able to make synaptic contact with the cell bodies of the latter cell type, in the way we know dopamine cell processes do (see below and amacrine cell chapter). The VGLUT3 amacrines appear to be in a good position to interact with OFF center ganglion cell, stained for MAP-1, dendrites as shown in Figures 3D, E and F.
Fig. 4 EM of VGLUT3 immunostained processes in the IPL of the rat retina.
Recent evidence from the metabolic mapping technique of Marc and Jones (2004) indicates that a dopaminergic amacrine cell type also has a content of glutamate. However, from the above evidence on VGLUT3 immunostaining it is clear that the dopaminergic type 1 cell does not use that particular vesicular glutamate transporter.
3. Gamma aminobutyric acid.
Fig. 5. Expression pattern of GABA immunoreactivity in human retina (78 K jpeg image)
4. Glycine.
The other classic inhibitory neurotransmitter glycine, accounts for most of the small-field types of amarine cell. All amacrine cells in the vertebrate retina can be accounted for by the two inhibitory neurotransmitters GABA and glycine (Marc et al., 1995). In addition one or more types of bipolar
cell are also thought to contain glycine in mammalian retinas including monkey
and human.
In Figure 6 it can be seen that the immunostaining for glycine is just
as strong in the inner plexiform layer as GABA staining. About the same number
of amacrine cells are revealed. However there is an addition of some small
bipolar cell bodies in the inner nuclear layer and the occasional large cell
body of a ganglion cell type in the ganglion cell layer (Crooks and Kolb,
1992).
Fig. 6. Expression pattern of Glycine immunoreactivity in human retina (78 K jpeg image)
Two morphological types of glycinergic amacrine cell can be demonstrated even
in immunocytochemical staining of the whole population of glycinergic amacrines
in human retina (Fig. 7). The less intensely stained cell has the morphological
features of the rod pathway AII amacrine cell (i.e lobular appendages and thick
apical dendrite arising from a mitral shaped cell body protruding down into the
neuropil of the IPL). Pourcho and Goebel (1985) showed quite clearly that
tritiated glycine accumulated in Golgi stained AII, A4, and A8 cells. The
latter cell was the most strongly glycinergic of the three small field amacrine
cells, so we suggest that this amacrine is also most intensely stained in the
human retina (Crooks and Kolb, 1992) (Fig. 7 below).
The classical inhibitory neurotransmitters, gamma aminobutyric acid (GABA)
occurs in many different varieties of amacrine cells and in one or more classes
of horizontal cell in most vertebrate retinas (Marc et al., 1995) There is
still some controversy over whether GABA is contained within horizontal cells
in monkey and human retina.
A valuable identification of individual cell types that contain GABA has come
from double staining techniques upon Golgi stained cell types (Pourcho and
Goebel, 1983). Thus we know now that A10, A13, A17, A19, and the
interplexiform cell accumulate GABA and probably use it as their primary
neurotransmitter. Some amacrine cell types also colocalize GABA with another
neurotransmitter. Thus the GABAergic A17 colocalizes serotonin, the
acetylcholine (starburst amacrine) colocalizes GABA and so does the dopamine
A18 cell (Vaney, 1990). Neuropetides (see later) are also commonly colocalized
with GABA i.e. substance P in A22 is almost certainly the secondary transmitter
to GABA as the primary. GABAergic amacrine cells and IPCs act upon bipolar,
amacrine and ganglion cell processes or cell bodies in the neuropils of the
retina via all the three varieties of GABA receptors (A, B and C types) but
the specifics of which receptors are associated with which morphological or
physiological subtype of cell, still needs elucidation.
Fig. 7 Expression of Glycine immunoreactivity in human amacrine cells (59 K jpeg image)
5. Dopamine is present in amacrine cells in the mammalian retina.
The neuromodulator dopamine is found in one or more types of amacrine cell in the mammalian retina. The most robustly stained dopaminergic cell after immunocytochemistry to the rate limiting enzyme of dopamine synthesis, tyrosine hydroxylase (Toh), is recognized as an A18 cell of the Golgi descriptions (Kolb et al., 1981, Kolb et al., 1992).
 Fig. 8. Wholemount view of a type 1 TOH+ amacrine cell (78 K jpeg image) |
 Fig. 9. Vertical section of a type 1 TOH+ amacrine cell (78 K jpeg image) |
A second type of dopamine amacrine cell has also been described in the monkey and human retinas (Mariani and Hokoc, 1988; Crooks and Kolb, 1992). The Type 2 CA cell has dendrites stratifying in stratum 3 of the IPL and in vertical views of Toh processed human retinas these dendrites can be seen quite clearly below those of the Type 1 (A18) dendritic plexus in stratum 1 (orange arrows, Fig. 9).
Type 1 dopamine cells provide ascending processes to the outer plexiform layer (see above) which are known to synapse on the GABAergic interplexiform cell (see previous chapter on feed-back loops).GABA and dopamine colocalize to the A18 cell type (Type 1 CA cell) and serotonin has also been found to co-exist in in the same amacrine cells in cat retina (Wässle and Chun, 1988).
Both D1 and D2 receptor types have been found on neurons of the inner and outer retina in many vertebrates. It is thought that the D1 receptor is particularly associated with cells that are coupled by gap junctions, because of dopamine's known action in cyclic AMP regulation of gap junction channels (Lasater and Dowling, 1985). Thus D1 receptors have been demonstrated in association with horizontal cells of the OPL and some amacrine cells of the IPL. D1 receptors are robust on ganglion cell bodies as well (personal observations), despite the fact that the dopamine amacrine cell is not known to make direct synapses upon ganglion cells. D2 receptors are also found in the retina associated with photoreceptors in the outer nuclear layer, outer limiting membrane and retinal pigment epithelium even. Also they are present in the IPL but the target cells in this neuropil are not well understood yet.
6. Acetylcholine.
The classic fast excitatory neurotransmitter of the peripheral nervous system,
acetylcholine (ACh), is found in a mirror symmetric pair of amacrine cells in
the vertebrate retina. In the rabbit such cells have been named starburst cell
(Famiglieti, 1983; Masland and Tauchi, 1986). One of the mirror pair occurs in
the amacrine cell layer with dendrites in sublamina a (OFF sublamina of
the IPL). The other of the pair has its cell body displaced to the ganglion
cell layer and its dendrites stratify in sublamina b (ON sublamina of
the IPL).
These ACh containing amacrine cells are common to almost all vertebrate
retinas and have been described morphologically in human retina too (Hutchins
and Hollyfield, 1987; Kolb et al., 1992) (see previous chapter on amacrine
cells). Both muscarinic and nicotinic receptors have been demonstrated in the
mammalian retina, particularly associated with transient phasic ganglion cells
(Y cells) (Keyser et al., 1989; Hughes, 1991) and effects of ACh and
antagonists on ganglion cell responses are documented but not well understood.
Fig. 10. ACh containing amacrine cell stained with Lucifer yellow (59 K jpeg image) 7. Serotonin.
There are two types of serotonin-accumulating amacrine cell in the rabbit
retina (Vaney, 1986). One of these is almost certainly the A17 cell or the
reciprocal amacrine cell of the rod system in the rabbit (see previous
chapters) (Fig. 11). However, in cat retina, a completely different amacrine cell type
stains with antibodies against serotonin. One cell type in cat is similar to
the wide-field cell A20, while the other may be the A18 or dopamine cell
(Wässle and Chun, 1988). Even where serotonin is strongly demonstrated
in these amacrine cells in rabbit retina, it is not thought to be the
neurotransmitter.
Serotonin co-exists with GABA, in the A17 cell and the latter is thought to be the releasable transmitter (Ehinger and Dowling, 1987; Vaney, 1990). A few cold-blooded vertebrates have a bistratified amacrine cell and a bipolar cell type that immunostain for serotonin (Schütte and Weiler, 1987; Hurd and Eldred, 1993).
8. Adenosine may be a retinal neurotransmitter.
The purine nucleotide, adenosine may be a neurotransmitter or neuromodulator
in the mammalian retina. Autoradiography and immunocytochemistry for adenosine
has revealed cell bodies in the amacrine and ganglion cell layers (Blazynski
and Perez, 1991). Probably most of these cells are amacrine cells but some in
the ganglion cell layer may be true ganglion cells. In human retina additional
cells that could be bipolar or horizontal cell label too. K+ and light evoked
release of adenosine can be measured in rabbit and chick retinas. And the
vertical pathway neurotransmitter glutamate can induce adenosine release from
[3H]-adenosine preloaded rabbit retina. Additionally some effects
of adenosine on the ERG generated in the retina and on the activity of ganglion
cell terminals in the superior colliculus have been recorded and the
information points to the strong likelihood that adenosine does play a
neurotransmitter role in the vertebrate retina (See review by Blazynski and
Perez, 1991). Adenosine colocalizes with GABA, acetylcholine and serotonin in
various retinas. Much more research is needed in this area.
9. Substance P occurs in an amacrine type and a ganglion cell type.
Substance P (SP) is a neuropeptide belonging to the tachykinin family that
include neurokinin A, neuropeptide K and neurokinin B, as well. Substance P is
thought to be a neurotransmitter or neuromodulator in the vertebrate retina
(See Kolb et al., 1995, for a review).
SP-IR amacrine cells appear to be of a single type in the human retina (Fig. 12, above). They are large-field cells with large cell bodies (16 um diameter)
lying in normal or displaced positions on either side of the inner plexiform
layer (IPL). Fig. 12. Substance P containing amacrine cell in human retina (59 K jpeg image)
In addition to the SP-IR amacrine cells, a ganglion cell type is immunostained
with SP (Fig. 13). Its 20- 22 um cell body gives rise to a radiate, sparsely-branched,
wide-spreading dendritic tree running in S3. Its dendrites and cell body become
enveloped by the more intensely SP-IR processes and boutons from the SP-IR
amacrine cell type (Fig. 13, fine arrows). The SP-IR ganglion cell type most resembles G21 of a Golgi
study. A ganglion cell type in rabbit retina has definitely been proved to
contain substance P. Such ganglion cells almost certainly colocalize a more
standard neurotransmitter like glutamate too (Brecha et al., 1987).
Fig. 13. Substance P containing ganglion cell in human retina (59 K jpeg image) 10. Other neuropeptides.
Immunostaining with antibodies against somatostatin has revealed a small population of neurons in the ganglion cell layer in the rabbit retina (Sagar, 1987). They are distributed only in the inferior retina and in the far peripheral circumference of the retina. However, in the monkey and human retinas these amacrines are more uniformly distributed. The somatostatin-IR amacrines have long fibers that distribute across the entire retina running in three plexuses in the middle and outer and inner strata of the inner plexiform layer (Fig. 14, from Marshak, 1989). In the human and monkey most of the somatostatin-IR cells have their cell bodies in the ganglion cell layer (Fig. 14) and they emit fibers or axon-like processes that can be measured running 20 mm across the entire retina (Sagar and Marshall, 1988). Because these axon like processes stay within the retina, not passing to the optic nerve, the somatostatin-immunoreactive cells are likened to the associational neurons of Cajal (1892).
Their sturdy, spiny and appendage-bearing dendrites stratify in
stratum 3 (S3) of the IPL, where many overlapping fine dendrites intermingle to
form a plexus of stained processes. Either cell bodies or primary dendrites
emit "axon-like" process which divides typically into two long, fine processes
that run in opposite directions for hundreds of microns in S5 and S3 before
disappearing as distinct entities in the stained plexus in S3. Long fine
dendrites also pass from the dendritic plexus to run in S5 and down to the
nerve fibre layer to end as large varicosities at blood vessel walls. In
addition fine processes are emitted from the dendritic plexus that run in S1,
and some pass up to the outer plexiform layer (OPL) to run therein for short
distances. The SP-IR amacrine cell has many similarities to thorny type 2
amacrine cells described in Golgi studies. SP amacrine cells co-localize GABA
as a neurotransmitter (Pourcho and Goebel, 1988).
Corticotropin releasing factor (CRF) is contained within a population of wide-field tristratified amacrines with long axon like processes, very similar in morphology to those containing somatostatin (Fig. 15) (Marshak, 1989). Colocalization of the two peptides has not been attempted yet but it seems probably that they are one and the same cell type.
Vasoactive Intestinal peptide (VIP) immunostains a population of amacrine cells that can be normally place in the INL or displaced to the ganglion cell layer (Fig. 16). They appear to have a medium size dendritic field and dendrites that branch diffusely through the middle strata of the IPL. They may be equivalent to the A12 type of Mariani (1990).
Amacrine cells that immunostain for neuropeptide Y are quite regularly stained in the primate and rodent retina. These amacrine cells have a characteristic sparsely branched wide-field dendritic tree with dendrites running in stratum 1 of the IPL (Fig. 17) (Marshak, 1989). Recent research wherby NPY amacrine cells can be selectively ablated indicates that these cells have a role in low spatial frequency tuning of certain large ganglion cell types (Sinclair et al., 2004). Both ON and OFF center ganglion cell types are said to be equally affected by loss of NPY amacrine cells, which is a strange finding considering the OFF stratum branching of these particuar amacrine cells. Presumably another chain of amacrine cells is involved in spatial tuning of ganglion in addition to the NPY type.
Using antibodies to the glycine extended form of cholecystokinin, Marshak and colleagues were able to demonstrate the presence of two different morphological types of amacrine cell and a single morphological type of bipolar cell in the monkey retina (Marshak, 1989; Kouyama and Marshak. 1992). The amacrines come as pairs that are either bistratified in the strata 2 and 4 and a larger bodied monstratified pair, again branching in either stratum 2 or 4 (Fig. 18). The blue cone specific bipolar cell is well characterized by CCK immunostaining and its distribution, contact with blue cones specfically and its probably ON center physiology is now well known (Kouyama and Marshak, 1992; Kolb et al., 1997) (See chapter on S-cone pathways).
11. NADPH-diaphorase staining and the possibility that there are nitric oxide containing neurons in the retina.
Nitric oxide is formed in many nerve cells of the peripheral and central
nervous system. It is known to play a role in second messenger cascades by
activating guanylyl cyclase and elevating cyclic GMP levels. Since many
neurotransmitters and transduction events utilize cyclic GMP in the retina
(notable phototransduction in the photoreceptors and activation of metabotropic
glutamate receptors) the idea that nitric oxide might play a key role in
retinal neurotransmission has been forwarded. Nitric oxide synthase the enzyme
required for synthesis of nitric oxide requires NADPH as a cofactor in the
cell. Thus the simple histochemical technique to reveal NADPH in a cell by the
reduction of tetrazolium salts has proved to be a good marker of neurons that
contain NADPH-diaphorase and hence possibly also nitric oxide synthase. An
antibody has been made against the synthase but staining and identification of
morphological cell types that contain this enzyme have been unsatisfactory to
date for the retina. Thus the NADPH-diaphorase histochemical technique is
still more reliable.
 Fig. 19. NADPH-diaphorase histochemical staining of an amacrine cell in monkey retina. |
 Fig. 20. Drawing from wholemount retina stained with NADPH-diaphorase of the commonly stained amacrine cell. |
In monkey retina, three types of amacrine cell and one type of ganglion cell appear clearly stained with NADPH-diaphorase. The commonest type is the one shown above (Figs. 19 and 20) and occurs at a maximum density of 280 cell/mm2 at 1 mm from the fovea (Cuenca, personal communication). It has a large cell body that lies either in the amacrine cell layer or can be displaced to the ganglion cell layer. The dendrites radiate out from the cell body like the spokes of a wheel, contain, many fine spines, and lie on one plane in stratum 3 of the IPL. Fine axon like processes arise from the main dendritic tree that is about 300 um in diameter to run for mm in all directions. The cell is probably the equivalent of a spiny amacrine described by Mariani (1990) and a cell type stained by Dacey as axon bearing (1989).
12. Amacrine cell populations and mosaics arrangements are revealed by neurotransmitter immunocytochemistry.
The summary table below lists the amacrine cell types that have now become
associated with particular neurotransmitter substances in the mammalian retina.
The list is compiled primarily from data of cat and rabbit retinas. However,
some clearly recognizable amacrine cell types of the monkey and human retina
have been included. The list is as yet incomplete concerning an exact
classification of each cell type by neurotransmitter signature because of the
difficulty of agreeing on correspondence between different authors
classification schemes and making cross species comparisons. The review article
by Vaney (1990) is the most comprehensive treatment on the subject of the
differences between cat and rabbit retina in this regard.
Immunocytochemical staining of amacrine cells, when done on wholemounts of
retina, can reveal every cell of the population that are immunoreactive to the
antibody used. Thus we are increasingly acquiring population maps and
distribution maps of all the different types of amacrine cells according to
neurotransmitter content. Most amacrine types are arranged in regular mosaics
and the individual cells have certain overlap characteristics that can be
calculated from nearest neighbor statistics. The cat and monkey amacrine
mosaics peak in cell density with closest packing of their smallest dendritic
trees in the fovea or area centralis. Then from center to periphery the neurons
distribute evenly in concentric rings of decreasing density and increasing
dendritic field sizes. The rabbit amacrine mosaics peak along the
horizontally-organized visual streak and fall off therefrom linearly into
superior and inferior retina (Vaney, 1990). Some of the more sparsely
distributed neurotransmitter types, have unique distributions. For example, the
somatostatin-immunoreactive associational neurons in rabbit retina are located
almost exclusively in inferior retina. The commonest amacrine cell type of the cat and rabbit retina is the
glycinergic AII amacrine (estimated 512,000 total in cat retina) followed by
the serotonin-accumulating amacrines (between 170,000 and 230,000 cells in
rabbit), cholinergic cells (approximately 130,000 in rabbit retina) and
substance P-containing cell types (39,000 cells in cat retina). Dopaminergic
amacrine cells are some of the lowest density populations of cells (3-5,000 in
cat; 6-8,000 in rabbit). Somatostatin occurs in a small population of only
1000 cells in rabbit retina.
Fig. 21. Summary diagram of the organization of neurotransmitters in the retina (59 K jpeg image)
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[General characteristics]
[Glutamate]
[Gamma aminobutyric acid]
[Glycine]
[Dopamine]
[Acetylcholine]
[Serotonin]
[Adenosine]
[Substance P]
[Other neuropeptides]
[Nitric oxide]
[Amacrine cell populations]
[References]
