Localization of AMPA-selective glutamate receptor subunits in the cat retina: a light- and electron-microscopic study

The distribution of AMPA-selective glutamate receptor subunits was studied in the cat retina using antisera against GluR1 and GluR2/3. Both antisera were localized in postsynaptic sites in the outer plexiform layer (OPL) as well as the inner plexiform layer (IPL). Immunoreactivity for GluR1 was seen in a subpopulation of OFF cone bipolar cells and a number of amacrine and ganglion cells. Within the IPL, processes staining for GluR1 received input from OFF and ON cone bipolar cells but not from rod bipolars. Labeling for GluR2/3 was seen in horizontal cells, an occasional cone bipolar cell, and numerous amacrine and ganglion cells. In the IPL, GluR2/3 staining was postsynaptic to cone bipolar cells in both sublaminae. AII amacrine cells which receive rod bipolar input were also labeled for GluR2/3. With both antisera, staining was limited to a single member of the bipolar dyad complex, providing morphological evidence for functional diversity in glutamatergic pathways.     

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.     

Distribution and developmental regulation of AMPA receptor subunit proteins in rat retina

PURPOSE: To learn more about a possible functional role of alpha-amino-3-hydroxy-5-methyl-4-isoxasole-propionate (AMPA) receptors in retinal development, the spatial distribution and temporal regulation of all AMPA receptor subunit proteins was studied in rats. METHODS: Immunohistochemistry was performed on retinal sections between embryonic days (E)20 and E21 and the adult stage by using specific antibodies against AMPA subunits GluR1 to 4. RESULTS: All AMPA subunits were expressed in the ganglion cell layer from E21 on. In the inner plexiform layer (IPL), discernible bands of labeling appeared at distinct retinal ages for the different subunits. GluR1 immunoreactivity (IR) was concentrated in two broad bands by postnatal day (P)3, whereas three bands were visible beginning on P9. Two bands were located in a region of the IPL where off-cells terminate, and one band was found in the innermost part of the IPL where on-cells terminate. In contrast, two bands of GluR2/3- and GluR4-IR in the IPL were only discernible beginning on P14 and seemed to be located between the bands of GluR1-IR. GluR2/3 and GluR4 were observed both in horizontal cells and in the outer plexiform layer from early developmental stages on. GluR1 was not found in the outer retina, indicating that horizontal and bipolar cell processes in the rat express AMPA receptors composed of subunits GluR2 to 4. Double-labeling experiments with cell-specific markers revealed the expression of subunits GluR1 to 4 in cholinergic and AII amacrine cells. CONCLUSIONS: AMPA receptors are expressed before synapse formation, indicating a role not only in fast signal transmission but also in the establishment of inner retinal circuits. The differences in spatial and temporal subunit expression suggest that different retinal cell types selectively express distinct types of AMPA receptors during development of the rat retina.     

Distribution of protein kinase C isoforms in the cat retina

Immunocytochemical localization was carried out for five isoforms of protein kinase C (PKC) in the cat retina. In common with other mammalian species, PKCalpha was found in rod bipolar cells. Staining was also seen in a small population of cone bipolar cells with axon terminals ramifying near the middle of the inner plexiform layer (IPL). PKCbetaI was localized to rod bipolar cells, one class of cone bipolar cell, and numerous amacrine and displaced amacrine cells. Staining for PKCbetaI was seen in three types of cone bipolar cells as well as in amacrine and ganglion cells. Immunoreactivity for both PKCepsilon and PKCzeta was found in rod bipolar cells; PKCepsilon was also seen in a population of cone bipolar cells and a few amacrine and ganglion cells whereas PKCzeta was found in all ganglion cells. Double-label immunofluorescence studies showed that dendrites of the two PKCbetaII-positive OFF-cone bipolar cells exhibit immmunoreactivity for the kainate-selective glutamate receptor GluR5. The third PKCbetaII cone bipolar is an ON-type cell and did not stain for GluR5. The retinal distribution of these isoforms of PKC is consistent with a role in modulation of various aspects of neurotransmission including synaptic vesicle release and regulation of receptor molecules.     

Distribution of GABA immunoreactivity in the cat retina: a light- and electron-microscopic study

The distribution of GABA-like immunoreactivity in the cat retina was studied through the use of preembedding immunocytochemistry for light microscopy and by postembedding immunogold techniques for electron microscopy. Staining was observed in both inner and outer plexiform layers. Approximately 30% of the somata in the amacrine portion of the inner nuclear layer were immunoreactive and included amacrine and interplexiform cells. Horizontal cells and a subpopulation of cone bipolar cells were also stained. In the ganglion cell layer, staining was observed in both small- and medium-sized neurons. GABA-labeled amacrine cells were presynaptic to somata of amacrine cells and to dendrites of amacrine, bipolar, and ganglion cells. Bipolar cells were a major target, receiving more than 60% of all labeled synapses in the inner plexiform layer. Many of these contacts were reciprocal synapses. These findings support a major role for GABA-labeled amacrines in providing feedback inhibition to bipolar cells in the inner retina.     

Differential cellular and subcellular distribution of glutamate transporters in the cat retina

Retrieval of glutamate from extracellular sites in the retina involves at least five excitatory amino acid transporters. Immunocytochemical analysis of the cat retina indicates that each of these transporters exhibits a selective distribution which may reflect its specific function. The uptake of glutamate into Muller cells or astrocytes appears to depend upon GLAST and EAAT4, respectively. Staining for EAAT4 was also seen in the pigment epithelium. The remaining transporters are neuronal with GLT-1alpha localized to a number of cone bipolar, amacrine, and ganglion cells and GLT-1v in cone photoreceptors and several populations of bipolar cells. The EAAC1 transporter was found in horizontal, amacrine, and ganglion cells. Staining for EAAT5 was seen in the axon terminals of both rod and cone photoreceptors as well as in numerous amacrine and ganglion cells. Although some of the glutamate transporter molecules are positioned for presynaptic or postsynaptic uptake at glutamatergic synapses, others with localizations more distant from such contacts may serve in modulatory roles or provide protection against excitoxic or oxidative damage.     

Development of glutamate receptor subunit 2 immunoreactivity in postnatal rat retina

Previous studies have shown that the expression of glutamate receptor subunits is developmentally regulated and have been implicated in processes of cell differentiation during postnatal life. The tissue localization and developmental pattern of the glutamate receptor 2 subunit of the alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionate (AMPA) receptor were investigated by means of immunohistochemistry and immunoblotting. Labeling of amacrine and ganglion cells and the inner plexiform layer appeared early during development, while glutamate receptor 2 subunit expression in the outer plexiform layer started after the first postnatal week. The distribution of labeling within the inner plexiform layer changed from nonorganized to laminated appearance prior to eye-opening. There was an increasing number of positive amacrine and ganglion cell somata during the first 2 weeks, but their number decreased considerably as the retina matured and were seen at least up to 35 days of postnatal development. Little labeling was found in the ganglion cell layer and in the inner plexiform layer of late postnatal and adult retina. Labeling in the outer plexiform layer and of bipolar cell somata appeared to increase in the developing retina. Glur2 labeling of these cells and the outer plexiform layer became discernible during the second postnatal week, and this labeling was present in the adult as well. Immunoblotting showed that GluR2 protein levels were similar at postnatal days 7 and 10, but slightly decreased between the second and fourth postnatal weeks. Our data imply that the immunological expression of glutamate receptor 2 subunit in the inner plexiform layer decreases as a function of age, and is correlated with developmental event(s) in the postnatal retina.     

Light and electron microscopical analysis of nitric oxide synthase-like immunoreactive neurons in the rat retina.

We have investigated the morphology of the NOS-like immunoreactive neurons and their synaptic connectivity in the rat retina by immunocytochemistry using antisera against nitric oxide synthase (NOS). In the present study, several types of amacrine cells were labeled with anti-NOS antisera. Type 1 cells had large somata located in the inner nuclear layer (INL) with long and sparsely branched processes ramifying mainly in stratum 3 of the inner plexiform layer (IPL). Somata of type 2 cells with smaller diameters were also located in the INL. Their fine processes branched mostly in stratum 3 of the IPL. A third population showing NOS-like immunoreactivity was a class of displaced amacrine cells in the ganglion cell layer (GCL). Their soma size was similar to that of the type 1 cells; however, their processes stratified mainly in strata 4 and 5 of the IPL. Labeled neurons were evenly distributed throughout the retina, and the mean densities were 57.0 +/- 9.7 cells/mm2 for the type 1 cells, 239.3 +/- 43.4 cells/mm2 for the type 2 cells and 121.2 +/- 27.5 cells/mm2 cells for the displaced amacrine cells. The synaptic connectivity of NOS-like immunoreactive amacrine cells was identified in the IPL by electron microscopy. NOS-labeled amacrine cell processes received synaptic input from other amacrine cell processes and bipolar cell axon terminals in all strata of the IPL. The most frequent postsynaptic targets of NOS-immunoreactive amacrine cells were other amacrine cell processes. Ganglion cell dendrites were also postsynaptic to NOS-like immunoreactive neurons in both sublaminae of the IPL. Synaptic outputs onto bipolar cells were observed in sublamina b of the IPL. In addition, a few synaptic contacts between labeled cell processes were observed. Our results suggest that NOS immunoreactive cells may be modulated by other amacrine cells and ON cone bipolar cells, and act preferentially on other amacrine cells.     

Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina

Electrical synapses or gap junctions occur between many retinal neurons. However, in most cases, the gap junctions have not been visualized directly. Instead, their presence has been inferred from tracer spread throughout the network of cells. Thus, tracer coupling is taken as a marker for the presence of gap junctions between coupled cells. AII amacrine cells are critical interneurons in the rod pathway of the mammalian retina. Rod bipolar cell output passes to AII amacrine cells, which in turn make conventional synapses with OFF cone bipolar cells and gap junctions with ON cone bipolar cells. Injections of biotinylated tracers into AII amacrine cells reveals coupling between the AII amacrine cell network and heterologous coupling with a variety of ON cone bipolar cells, including the calbindin-positive cone bipolar cell. To directly visualize gap junctions in this network, we prepared material for electron microscopy that was double labeled with antibodies to calretinin and calbindin to label AII amacrine cells and calbindin-positive cone bipolar cells, respectively. AII amacrine cells were postsynaptic to large vesicle-laden rod bipolar terminals, as previously reported. Gap junctions were identified between AII amacrine cells and calbindin-positive cone bipolar cell terminals identified by the presence of immunostaining and ribbon synapses. This represents direct confirmation of gap junctions between two different yet positively identified cells, which are tracer coupled, and provides additional evidence that tracer coupling with Neurobiotin indicates the presence of gap junctions. These results also definitively establish the presence of gap junctions between AII amacrine cells and calbindin bipolar cells which can therefore carry rod signals to the ON alpha ganglion cell.     

Wide-field cone bipolar cells and the blue-ON pathway to color-coded ganglion cells in rabbit retina

Wide-field cone bipolar cells with sparse dendritic branching and proposed connectivity to blue cones were first identified in rabbit and cat. In rabbit, these were subdivided into type a (wa) and type b (wb), with axonal branching in sublamina a, and sublamina b, respectively, of the inner plexiform layer (IPL). Recent studies in rabbit support the earlier hypothesis of exclusive blue/short wavelength cone connectivity for both types. The homologues of wb cells (but not wa cells) have been identified in other mammals. The axonal branching of wa cone bipolar cells is shown to co-stratify with the dendrites of the "fiducial," type a starburst amacrine cell, although a few branches extend into sublamina b. The axon terminal of wb cone bipolar cells is shown to be narrowly stratified in stratum 5alpha, deep to the dendrites of the type b starburst amacrine cell. Rabbit ganglion cells postsynaptic to wa cells are unknown, but may include class III.2a cells, similarly stratified in the IPL. The wb axon terminal is shown here to co-stratify with and to make close, likely synaptic, contacts with the dendrites of a recently described morphological subtype of class II ganglion cell in rabbit retina, IIb2. Recent morpho-physiological correlation indicates that class IIb2 cells correspond to the blue-ON-center-X or ON-brisk-sustained ganglion cells, defined physiologically in rabbit. In contrast, the wb cell in cat retina must innervate the physiologically identified blue-ON-center-sluggish-sustained ganglion cell. In monkey retina, the wb-like bipolar cells apparently innervate a small, partly bi-stratified ganglion cell. Mammals share a common pathway from short-wavelength-sensitive (S/blue) cone photoreceptors to ON-center ganglion cells in sublamina b of the IPL, in the form of wb or wb-like cone bipolar cells, but the type of ganglion cell innervated appears to be particular, and may serve different functional roles in different mammalian orders.     

Anatomical pathways for color vision in the human retina

The major neurons and neural circuits that are involved in the transmission of color signals through the human retina to produce the color and spatially opponent P cell or midget ganglion cell responses are described. The older findings of single cone to midget bipolar connectivity is reviewed, and the single midget bipolar cell to midget ganglion cell connectivity as revealed by a recent serial section electron microscope study is described in detail. Our present knowledge concerning the discrimination of the blue-cone subtype from the other longer wavelength cones in the human at the outer plexiform layer is summarized, and our most recent findings concerning horizontal cell connectivity to the different spectral types of cones are discussed. Finally, a hypothetical pathway is proposed for color-opponent surrounds of midget ganglion cells using both horizontal cells at the outer plexiform layer and amacrine cell pathways at the inner plexiform layer.     

Synaptic connectivity of two types of recoverin-labeled cone bipolar cells and glutamic acid decarboxylase immunoreactive amacrine cells in the inner plexiform layer of the rat retina.

We investigated the synaptic connectivity of two populations of recoverin-labeled bipolar cells and GABAergic neurons in the inner plexiform layer (IPL) of the rat retina. Two types of cone bipolar cells, type 2 and type 8, were stained with anti-recoverin antibodies, and GABAergic neurons were stained with anti-glutamic acid decarboxylase (GAD) antibodies. Type 2 cone bipolar axons received synaptic input from amacrine cell processes in 177 cases; among these amacrine cell processes, 92 processes (52.0%) were GAD-like immunoreactive. A total of 159 amacrine cell processes, which are presynaptic to type 8 cone bipolar cells, were observed. Among these processes, 117 processes (73.6%) were GAD-like immunoreactive. The postsynaptic elements at the ribbon synapses of recoverin-labeled cone bipolar cells were observed in 482 processes. In both type 2 and type 8 cone bipolar cells, the major output was to amacrine cell processes. At the ribbon synapses of the type 2 cone bipolar cells, 224 of the postsynaptic profiles were amacrine cell processes, 97 processes (43.3%) were GAD-like immunoreactive. In type 8 cone bipolar cells, 45 processes (30.2%) of 149 amacrine cell processes were GAD-like immunoreactive. Our results provide morphological evidence that GABA is a major transmitter involved in the visual processing of type 2 and 8 cone bipolar cells and GABA may have a stronger influence on type 8 cone bipolar cells than type 2 cone bipolar cells in the IPL of the rat retina.     

Synaptic organization of GABAergic amacrine cells in the salamander retina

The synaptic organization of GABA-immunoreactive (GABA-IR) amacrine cells in the inner plexiform layer (IPL) of salamander retina was studied with the use of postembedding immuno-electron microscopy. A total of 457 GABA-IR amacrine synapses, with identified postsynaptic elements, were analyzed on photomontages of electron micrographs covering 3,618 microm2 of the IPL. GABA-IR amacrine synapses were distributed throughout the IPL, with a small peak at the proximal margin of sublamina a. The majority of the output targets (81%) were GABA(-) neurons. Most of the contacts were simple synapses with one postsynaptic element identified as a process of an amacrine cell (55%), bipolar cell (19%) or ganglion cell (26%), and serial synapses were very rare. Of the 89 postsynaptic bipolar terminals, 63% participated in a reciprocal feedback synapse with the same presynaptic GABA-IR amacrine profile. There appeared to be no preference between GABA-IR amacrine contacts with rod- or cone-dominated bipolar cells (9.1% vs. 8.9%) or in the total number of amacrine synapses in sublaminas a and b (52% vs. 47%). The preponderance of amacrine cell input to bipolar cells in the OFF layer was derived from GABA-IR cells. These findings provide ultrastructural support to the existing physiological studies regarding the functional roles of the GABAergic amacrine cells in this species. Our results have added to the data base demonstrating that, in contrast to mammals, GABA-IR amacrine cells in amphibians and other nonmammals contact other amacrine cells more frequently, suggesting greater involvement of GABAergic amacrine cells in modulating lateral inhibitory pathways.     

Amacrine and bipolar inputs to midget and parasol ganglion cells in marmoset retina

Retinal ganglion cells receive excitatory synapses from bipolar cells and inhibitory synapses from amacrine cells. Previous studies in primate suggest that the strength of inhibitory amacrine input is greater to cells in peripheral retina than to foveal (central) cells. A comprehensive study of a large number of ganglion cells at different eccentricities, however, is still lacking. Here, we compared the amacrine and bipolar input to midget and parasol ganglion cells in central and peripheral retina of marmosets (Callithrix jacchus). Ganglion cells were labeled by retrograde filling from the lateral geniculate nucleus or by intracellular injection. Presumed amacrine input was identified with antibodies against gephyrin; presumed bipolar input was identified with antibodies against the GluR4 subunit of the AMPA receptor. In vertical sections, about 40% of gephyrin immunoreactive (IR) puncta were colocalized with GABAA receptor subunits, whereas immunoreactivity for gephyrin and GluR4 was found at distinct sets of puncta. The density of gephyrin IR puncta associated with ganglion cell dendrites was comparable for midget and parasol cells at all eccentricities studied (up to 2 mm or about 16 degrees of visual angle for midget cells and up to 10 mm or >80 degrees of visual angle for parasol cells). In central retina, the densities of gephyrin IR and GluR4 IR puncta associated with the dendrites of midget and parasol cells are comparable, but the average density of GluR4 IR puncta decreased slightly in peripheral parasol cells. These anatomical results indicate that the ratio of amacrine to bipolar input does not account for the distinct functional properties of parasol and midget cells or for functional differences between cells of the same type in central and peripheral retina.     

Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis, I: Gamma-aminobutyric acid.

The inhibitory amino-acid neurotransmitter, gamma-aminobutyric acid (GABA), was localized in the pure cone retina of the lizard Anolis carolinensis by autoradiographic and immunocytochemical techniques. Uptake of [3H]-GABA labeled horizontal cells, amacrine cells, numerous cells in the ganglion cell layer, both plexiform layers, and the nerve fiber layer. Label in the inner plexiform layer showed distinct lamination. The pattern of GABA immunoreactivity was similar to the pattern of [3H]-GABA uptake, although some differences, particularly in labeling of amacrine and ganglion cells, were observed. Immunocytochemistry revealed endogenous stores of GABA in a set of horizontal cells, amacrine cells, and cells in the ganglion cell layer. Both plexiform layers were labeled by the GABA antisera. Labeling in the inner plexiform layer (IPL) was highly stratified and GABA-immunoreactive strata were present in both sublaminae a and b. Six subtypes of conventionally placed GABA-immunoreactive amacrine cells and one displaced amacrine cell subtype were identified. Three of the six conventional amacrine cell subtypes were of pyriform morphology and three subtypes were of multipolar morphology. GABA-immunoreactive interstitial cells also were observed. Under certain conditions the GABA antiserum labeled the cones. Etching the resin eliminated cone labeling, suggesting that GABA in the cones is present in a labile pool, unlike GABA in horizontal or amacrine cells, or the observed labeling was not due to endogenous GABA. Cones did not demonstrate [3H]-GABA uptake.     

Immunolocalization of metabotropic glutamate receptors 1 and 5 in the synaptic layers of the chicken retina

We have examined the distribution of metabotropic glutamate receptors (mGluRs) 1 and 5 in the adult chicken retina using preembedding immuno-electronmicroscopy. Immunoreactivity for mGluRs 1 and 5 was found in both the outer plexiform layer (OPL) and the inner plexiform layer (IPL). For mGluR1, OPL labeling was observed at cone pedicles and horizontal and bipolar cell processes. In the IPL, mGluR1 labeling could be found on bipolar cell terminals, as well as postsynaptic processes, including amacrine cell processes. Neither presynaptic nor postsynaptic elements were labeled at rod synapses. For mGluR5, OPL labeling was associated with cone pedicles as well as bipolar and horizontal cell processes. As for mGluR1, rod synapses were unlabeled. In the IPL, labeling for mGluR5 was found on bipolar cell terminals and amacrine cell processes. The presynaptic expression of these receptors in the OPL was confirmed at the light level by double-labeling experiments with SV2. The distributions of mGluRs 1 and 5 indicate that they have the potential to regulate function in both synaptic layers. Furthermore, the similar expression patterns for these two receptors indicate that they might be co-expressed and thus have the potential to interact functionally.     

Glycine receptor immunoreactivity is localized at amacrine synapses in cat retina.

Immunocytochemical techniques were used to localize strychnine-sensitive glycine receptors in cat retina. Light microscopy showed staining in processes ramifying throughout the inner plexiform layer and in cell bodies of both amacrine and ganglion cells. At the electron-microscopic level, receptor immunoreactivity was seen to be clustered at sites postsynaptic to amacrine cells. In contrast, bipolar cells were neither presynaptic nor postsynaptic elements at sites of glycine receptor staining. Double-label studies verified the presence of glycine immunoreactivity in amacrine terminals presynaptic to glycine receptors. These findings support a role for glycine as an inhibitory neurotransmitter in amacrine cells.     

左旋精氨酸对兔眼AⅡ无长突细胞与开放性视锥型双极细胞间示踪剂藕连的调控研究

目的　探讨兔眼视网膜AⅡ无长突细胞 (AⅡamacrinecell,AⅡ AC)和开放性视锥型双极细胞 (onconebipolarcell,ON CB)间缝隙连接通道的相对通透性及左旋精氨酸对通道的调节。方法　单个AⅡ AC显微注射神经生物素 (neurobiotin ,NB)后 ,采用共焦显微镜测定以上两类异源型细胞群中NB的分布 ,并用 4mmol/L左旋精氨酸对其进行调节。然后用兔抗Calretinin抗体对注射后的视网膜进行免疫组织化学染色。结果　藕连的ON CB中的NB的浓度低于藕连的AⅡ AC中NB的浓度。与藕连的AⅡ AC比较 ,左旋精氨酸选择性的减少了与AⅡ AC藕连的ON CB中的NB的浓度(t=2 5 11,P <0 0 5 )。AⅡ AC被Calretinin抗体染色阳性。结论　相对于AⅡ AC和ON CB间可能的异源型缝隙连接 ,NB较易通过AⅡ AC间的同源型缝隙连接。左旋精氨酸可能使cGMP浓度升高而作用于双极细胞侧的缝隙连接 ,选择性的减少了这种双极细胞的示踪剂标记。     

Anatomical and electrophysiological evidence for GABAergic bipolar cells in tiger salamander retina

Our previous work showed that about 12% of bipolar cells in salamander retina synthesize and take up gamma-aminobutyric acid (GABA), are GABA transporter (GAT)-immunoreactive, and respond with a GAT current to extracellularly applied GABA, suggesting that these bipolar cells use GABA, in addition to glutamate, as a neurotransmitter. Further support for this idea was obtained in this study by use of immunogold electron microscopy and whole-cell patch clamp electrophysiology. Ultrastructural analysis showed that amacrine cell and ganglion cell processes were postsynaptic to GABA-immunoreactive synapses made by bipolar cell axon terminals. Whole-cell recordings were obtained from amacrine and ganglion cells in response to activation of bipolar cells by puffing KCl at their dendrites in the outer plexiform layer. Inhibitory postsynaptic currents were observed in several third order neurons, even after blocking the excitatory postsynaptic responses, generated in the inner plexiform layer, with a combined application of NMDA and non-NMDA receptor antagonists, AP-5 and CNQX. These ultrastructural and electrophysiological data support our previous neurochemical results, and suggest that the retinal through-information pathway in salamander includes both inhibitory GABAergic as well as excitatory glutamatergic synaptic mechanisms.