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Excitatory amino acid transporters of the salamander retina: identification, localization, and function.

The rapid re-uptake of extracellular glutamate mediated by a family of high-affinity glutamate transporter proteins is essential to continued glutamatergic signaling and neuronal viability, but the contributions of individual transporter subtypes toward cellular physiology are poorly understood. Because the physiology of glutamate transport in the salamander retina has been well described, we have examined the expression and function of glutamate transporter subtypes in this preparation. cDNAs encoding five distinct salamander excitatory amino acid transporter (sEAAT) subtypes were isolated, and their molecular properties and distributions of expression were compared. We report evidence that at least four distinct sEAAT subtypes are expressed in glial (Müller) cells. In addition, four of the five transporter subtypes are localized in neurons throughout the retina. The brightest immunostaining was seen in the synaptic regions of the inner and outer plexiform layers and in the outer nuclear layer. Using electrophysiological measurements in the Xenopus oocyte expression system, we also examined the pharmacology and ionic dependence of the four expressing transporter subtypes that make it possible to distinguish, on the basis of functional behavior, among the various subtypes. Although no simple correlation between transporter subtype and retinal cell physiology can be made, the diverse population of sEAAT transporter subtypes with unique localization and functional properties indicates that glutamate transporters play a wide variety of roles in retinal function and are likely to underlie both the uptake of glutamate by Müller cells and the glutamate-elicited chloride conductance involved in signal transduction by photoreceptors and bipolar cells.

ATP-Binding Cassette Transporters↗

The relation between the axial complex of meiotic prophase chromosomes and chromosome pairing in a salamander (Plethodon cinereus).

An investigation of the structure of meiotic chromosomes from primary spermatocytes of two salamanders, Plethodon cinereus and Desmognathus fusca, has been made using correlated light and electron microscopy. Feulgen squashes were compared with stained sections and these related to adjacent thin sections in the electron microscope. A transition from the familiar cytological preparation to the electron image was thus effected. A linear complex consisting of three parallel strands has been observed with the electron microscope, passing along the central axis of primary spermatocyte chromosomes. The complex is similar to that found in comparable chromosomes from at least a dozen animal species. The structure in Plethodon is described in detail. Synapsis has been positively identified as the stage of meiotic prophase at which the complex occurs. Thus the complex is a part of bivalent chromosomes. It has not been seen in other stages or other divisions and is thus thought to be exclusively of synaptic occurrence. The term synaptinemal complex is suggested for the entire structure. By virtue of the material condensed around it, the complex is also seen in the light microscope where it appears as a fine, densely Feulgen-positive central core along the chromosome. The complex is thus closely associated with DNA, if not at least in part, composed of it. In the stages studied, homologous chromosomes are not always completely paired. The lateral elements of the complex separate and follow the single chromosome axes at these points. The central element disappears and thus may be a phenomenon of pairing. It is concluded that the lateral elements of the synaptinemal complex may more correctly be a "core" of the single meiotic prophase chromosome, possibly being concerned with its linear organization.

Animals↗

Natural triploidy in salamanders related to Ambystoma jeffersonianum.

Female salamanders with large erythrocytes and erythrocyte nuclei produced triploid larvae; females with small erythrocytes and erythrocyte nuclei produced diploid larvae. Larval chromosome counts, dimorphism in cell size, and sex inheritance indicate distinct, persisting populations of triploid females in parts of the range of the Ambystoma jeffersonianum complex.

Ambystoma↗

Climatic data sources and limitations of ecological niche models impact the estimations of historical ranges and niche overlaps in distantly related Korean salamanders.

BACKGROUND: Ecological niche models (ENMs) and analyses of niche overlap/divergence have become popular methods in ecology and evolutionary biology. These analyses rely on environmental data available from several databases. However, the influence of data sources on these analyses is rarely tested. Here, we test the impact of climatic data choice on the prediction of current and Plio-Pleistocene suitable habitats for two distantly related, but broadly sympatric, salamanders endemic to the Korean Peninsula. We ran MaxEnt separately on WorldClim and CHELSA climate data. We then hindcasted ENMs to five time periods of the Plio-Pleistocene, bracketing the estimated intraspecific divergence times for these species. We then quantified the differences in predictions between WorldClim- and CHELSA-based models. Also, given the sympatry and similar habitat requirements of the two species, we tested for niche overlaps using niche identity and background tests and tested the sensitivity of the results to climatic data choice. RESULTS: The ENMs successfully predicted contemporary suitable habitats for the two species. However, the predictions were highly sensitive to climatic data choice as well as variable combinations. The hindcasted ENMs produced contrasting predictions depending on the choice of climatic dataset and failed to predict suitable habitats for some Pleistocene time periods regardless of the climatic data choice. The niche analyses were also sensitive to climatic data choice, with results suggesting either niche overlaps or divergence depending on the climatic dataset used for the analyses. CONCLUSIONS: Our study highlights the influence of climatic data choice on the outcomes of ENMs and niche analyses. Our results also underscore the limitations of macroclimate-based ENMs, especially when the species is likely buffered from macroclimatic changes by microhabitat. We argue for the need for additional ecological, ecophysiological, and population genomic studies to better understand the range formation of these enigmatic species.

Animals↗

Immunocytochemical localization of gamma-aminobutyric acid plasma membrane transporters in the tiger salamander retina.

Gamma-aminobutyric acid (GABA) plasma membrane transporters (GATs) play an important role in regulating GABA neurotransmission in the nervous system. The distribution of two GATs, GAT 1 and GAT 3, in salamander retina was investigated by using affinity-purified polyclonal antisera directed to the predicted C-terminals of rat GAT 1 and rat GAT 3. GAT 1-immunoreactivity (-IR) was found in type IB and IIB orthotopic bipolar cells (BCs) located in the distal and middle of the inner nuclear layer (INL), respectively; in type IIA and IA amacrine cells (ACs) located in the middle and proximal INL, respectively; and in interplexiform cells and cells in the ganglion cell layer (GCL). No detectable staining was found in horizontal cells (HCs) or in structures resembling Müller cells. GAT 1-immunoreactive fibers were present in the outer plexiform layer (OPL) and inner plexiform layer (IPL) in three bands corresponding to the three bands previously reported to be GABA-IR. GAT 3 antibodies labeled fewer cells and cell types than GAT 1 antibodies. GAT 3-IR was localized to type IIA and IA ACs and cells in the GCL, but not to BCs, HCs, or Müller cell-like structures. There was weak labeling of the OPL and stronger labeling of the IPL, with three distinct bands at the same depth as observed with GAT 1-IR. Double-labeling showed that the majority of GAT 1-IR BCs (88%), ACs (88%), and cells in the GCL (78%) colocalized with GABA-IR. The present study provides the first direct evidence of the expression of two GAT subtypes in neurons of nonmammalian retinas. These transporters could regulate GABA neurotransmission by reuptake and termination of GABA's action and, perhaps, by GABA release mechanisms. The presence of GAT 1-IR/GABA-IR bipolar cells further supports our earlier observations that a subgroup of orthotopic bipolar cells are likely to be GABAergic.

Ambystoma↗

Automatic characterization and classification of ganglion cells from the salamander retina.

The classification of retinal ganglion cells according to their morphological features is addressed by using a comprehensive set of shape measures and several clustering strategies. The morphological features considered include many common measures (such as dendritic radii and the number of dendritic segments) and three new quantifiable measures: 1) the area of influence of the dendritic tree as calculated in an operator-independent manner by using Minkowski sausages; 2) the complexity of tortuousity along each dendritic segment as represented by the 3D bending energy; and 3) the coverage factor as calculated by using the Bouligand-Minkowski fractal dimension, which is more accurate than the commonly used box-counting algorithm. We evaluated four clustering approaches including the k-means and Ward's hierarchical clustering methods. By using these highly quantifiable methods to group the cells into classes, the present work has extended and reassessed the analysis of 68 ganglion cells from the tiger salamander previously classified by Toris et al. ([1995] J. Comp. Neurol. 352:535-559). Though substantiating the number of classes (5) previously proposed by Toris et al., the results obtained here indicate a number of discrepancies among the members of each class, especially regarding the border between two classes, originally called the medium simple and the medium complex cells. Such an effect has motivated the proposal of new names for the medium simple and medium complex classes, now called small highly complex and medium cells, respectively. Also included in the present article are comprehensive statistics of each class, correlations among all the adopted shape measures, and examples of the cells from each class. The resultant classes that emerged were compared using their electrotonic characteristics and physiological profiles.

Ambystoma↗

Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. II: intracellular recording and labeling experiments.

In the plethodontid salamanders Plethodon jordani and P. glutinosus, the morphology and axonal projections of 140 tectal neurons and their responses to electrical optic nerve stimulation were determined by intracellular recording and biocytin labeling. Six types of neurons are distinguished morphologically. TO1 neurons have wide dendritic trees that arborize mainly in tectal layers 1 and 3; they project bilaterally to the tegmentum and contralaterally to the medulla oblongata. TO2 neurons have very wide dendritic trees that arborize mainly in layers 2 and 3; axons project bilaterally or unilaterally to the pretectum and thalamus and ipsilaterally to the medulla oblongata. TO3 neurons have very wide and flat dendritic trees confined to layers 3-5; some have the same axonal projection as TO2 neurons, whereas others have descending axons that reach only the level of the cerebellum. TO4 neurons have narrower dendritic trees that arborize in layers 2 and 3; they project to the ipsilateral pretectum, thalamus, and medulla oblongata. TO5 neurons have dendritic trees that arborize in layers 1 and 2 or 1-3 and project bilaterally or unilaterally to the pretectum and thalamus. TO-IN are interneurons, with a number of subtypes with respect to variations in dendritic arborization pattern. TO1-TO5 neurons generally have short latencies of 2-16 ms (average = 8.4 ms) at electrical optic nerve stimulation; first responses are always excitatory, often followed by inhibition. They are likely to be mono- or oligosynaptically driven by retinal afferents. TO-IN interneurons have long latencies of 20-80 ms (average = 38.6 ms) and appear to receive no direct retinal input. With their specific dendritic arborization, consequent dominant retinal input, specific axonal projections, the different types of tectal projection neurons constitute separate ascending and descending visual pathways. Hypotheses are presented regarding the nature of the information processed by these pathways.

Animals↗

Experimental analysis of character coupling across a complex life cycle: pigment pattern metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum.

Developmental relationships among characters are expected to bias patterns of morphological variation at the population level. Studies of character development thus can provide insights into processes of adaptation and the evolutionary diversification of morphologies. Here I use experimental manipulations to test whether larval and adult pigment patterns are coupled across metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum (Ambystomatidae). Previous investigations showed that the early larval pigment pattern depends on interactions between pigment cells and the lateral line sensory system. In contrast, the results of this study demonstrate that the major features of the adult pigment pattern develop largely independently of both the early larval pattern and the lateral lines. These results suggest that ontogenetic changes that occur across metamorphosis decouple larval and adult pigment patterns and could thereby facilitate independent evolutionary modifications to the patterns during different stages of the life cycle.

Ambystoma↗

Description of the postcloacal glands of Plethodon cinereus, the red-backed salamander, during bouts of scent marking.

Plethodon cinereus, the red-backed salamander, is a small territorial vertebrate that defends refugia located on the forest floor. As a component of territorial defense, these animals use scent marks to advertise their refugia. Behavioral evidence indicates that scent marks are produced by the postcloacal glands located on the ventral surface of the tail just posterior to the cloaca. We placed animals on unmarked substrates and recorded changes in serous acini from the postcloacal and shoulder region over a 48-h period. Within the first hour there was an increase in the number of acini filled with secretory product in the postcloacal region. At 12 h the number of full acini decreased and the number of empty acini increased. By 24 h the number of empty acini had decreased and the number of renewing acini containing secretory cells producing product had increased. By 48 h the ratio of full to empty to renewing acini was similar to those observed at the start of the study. In the shoulder region, no significant changes in the ratio of full to empty to renewing acini were observed. Observations of the serous acini within the postcloacal region and the shoulder region indicate that the mode of secretory production is holocrine. These findings are additional evidence that the postcloacal glands are the site of scent mark production.

Animals↗

Heterogeneity in the distal nephron of the salamander (Ambystoma tigrinum): a correlated structure function study of isolated tubule segments.

Studies on isolated perfused tubules of the tiger salamander (Ambystoma tigrinum) have shown that the distal nephron is heterogeneous with respect to function (Stoner, 1977). In this study, the initial portion of the distal tubule (diluting segment) exhibited a voltage, positive in the lumen, and a net absorption of chloride. Since the chloride was transported against an electro-chemical gradient, its transport was active. More distad, the junctional segment exhibited a lumen-negative voltage and sodium, rather than chloride, was transported actively. More recently Delaney and Stoner (1981) have demonstrated in vitro that the collecting duct of this species also has a lumen-negative voltage which is probably associated with active sodium reabsorption. The primary objective of the present paper was to correlate the morphology of the diluting and junctional segments of the Ambystoma distal tubules with the physiologic data from the same isolated perfused tubules. The results indicate that the morphological heterogeneity previously demonstrated in distal tubules of Necturus exists with respect to both structure and function in Ambystoma. The cell types found in the amphibian distal nephron appear to be homologous to those seen in the mammalian nephron.

Animals↗

Morphological relations between the receptor neurons, sustentacular cells and Schwann cells in the olfactory mucosa of the salamander.

The morphological characteristics of olfactory receptor neurons and their relations to the sustentacular cells and to the sheath cells of Schwann in the olfactory mucosa of the salamander (Ambystoma maculatum et tigrinum) were studied using a modification of the rapid Golgi technique. The bipolar receptor neurons had a fusiform-shaped cell body whose apical pole gave rise to a surface-reaching dendrite and a basal pole which gave rise to an axon. The length and width of the dendrite, although variable, were positively correlated with the relative depth at which the cell body was located in the sensory epithelium. Beyond the initial segment, the axon had a sinuous course prior to its entrance into the lamina propria. Within the lamina propria, the axons were associated with the sheath cells of Schwann to form the olfactory nerve fascicles. The processes of adjacent sheath cells formed an elaborate network of continuous cavities through which the axons coursed. Two morphologically distinct varieties of sustentacular cells, designated types I and II, were found in the sensory epithelium. Both types had a columnar profile consisting of an elongated cell body, a central stalk, and a basilar expansion of the stalk found at the junction of the epithelium with the lamina propria. The central stalk of type I sustentacular cells was unbranched, whereas that of type II cells gave rise to riblike processes from which cytoplasmic veils extended to envelop the cell bodies of receptor neurons. The basilar expansions were found in close apposition to the wall of capillaries or to acinar cells of Bowman's glands located in the most superficial region of the lamina propria. The morphological relationships and possible interdependencies among receptor neurons, the types of sustentacular cells, and the sheath cells are discussed.

Animals↗

A practical method for staging metamorphosis in the tiger salamander Ambystoma tigrinum.

The aim of this study was to develop a set of practical metamorphic stages for the tiger salamander Ambystoma tigrinum that would 1) provide an early and quantifiable marker of the onset of metamorphosis and 2) not be dependent on knowledge of maximal values of gill length or tail height. Twenty morphological parameters were obtained from Ambystoma tigrinum larvae as they progressed through laboratory-induced metamorphosis (21 degrees C, continuous light). These parameters included measures of body weight, gill length, and tail height. Initiation or duration of metamorphosis could not be predicted when parameters were expressed relative to the number of days larvae were held in laboratory conditions. Early phases of metamorphosis were characterized by regression of the lower tail fin. Selected morphological parameters were expressed relative to the day on which each subject exhibited complete regression of the lower fin. This technique made it possible to order these parameters into a progressive series of metamorphic phases. Seven stages of metamorphosis were derived from this series, ranging from larvae (stage I) to complete regression of the gills (stage VII). Application of these stages does not require prior knowledge of maximal (initial) values of gill length or tail height.

Ambystoma↗

Ultrastructural characteristics of sustentacular cells in control and odorant-treated olfactory mucosae of the salamander.

The ultrastructural characteristics of five morphologically distinct regions of sustentacular cells in the salamander olfactory mucosa are described. 1) The apical region was characterized by a microvillar surface that lay below the level of the olfactory knob of olfactory receptor neurons and contained endosome-like vesicles and a filamentous array at the level of the zonula adherens. 2) The supranuclear region contained rough and smooth endoplasmic reticulum, a Golgi complex, and secretory vesicles. Few sustentacular cells showed morphological signs of secretion, suggesting a low rate of baseline secretory activity. 3) The nuclear region contained the cylindrical nucleus surrounded by a thin band of cytoplasm containing bundles of filaments. 4) The central stalk contained filamentous arrays, Golgi-like cisternae, multivesicular bodies, and peroxisomes. Cytoplasmic veils that extended from the central stalk contained filamentous aggregates. 5) The basilar expansion had a complex series of lateral and basal folds. The lateral folds enveloped extracellular material and nonmyelinated axons of the receptor neurons. The basal folds formed complex interdigitations with the basal lamina, particularly in regions occupied by blood vessels and the acini of Bowman's glands in the subjacent lamina propria. These characteristics, and the presence of endosome-like vesicles and mitochondria, suggest that the basilar expansion is metabolically active and participates in cellular transport of material. Treatment with the odorant 2-isobutyl-3-methoxypyrazine caused ultrastructural changes in the apical and supranuclear regions that were associated with secretion and in the basilar expansion region that were indicative of an increase in metabolic and transport activity.

Animals↗

Comparative anatomy and phylogeny of the cloacae of salamanders (Amphibia: Caudata). IV. Salamandridae.

Cloacae were examined from male and female salamanders representing 12 genera and 22 species in the Salamandridae. All female salamandrids possess numerous sperm storage glands, spermathecae, in the roof of the cloaca, but intergeneric variation exists in the occurrence of additional cloacal glands. Pleurodeles and Tylototriton possess both vent and anterior ventral glands, and secondary loss has occurred of vent glands in all other genera and anterior ventral glands in Chioglossa, Cynops, Paramesotriton, and Triturus The most highly derived cloaca occurs in Euproctus asper, in which the cloacal tube extends through a conical projection, and ventral glands secrete onto the dorsolateral surface of the projection rather than into the cloaca. Marked intergeneric variation occurs in males in conformation of the cloacal cavities and in extent of the dorsal gland. In Cynops, Euproctus, Pachytriton, Paramesotriton, Taricha, and Triturus, the pseudopenis (a broad, posteriorly projecting evagination of the dorsal roof) fills much of the cavity of the anterior cloacal chamber. In most salamandrids, distal ends of the dorsal glands occur lateral to pelvic glands in the anterior end of the cloaca, and dorsal gland tubules descend to secretory sites at the posterior end of the vent. Salamandra and Mertensiella possess a unique, bifurcated dorsal gland in which distal ends of tubules lie dorsal to the other cloacal glands, and proximal ends curve ventrally in the anterior end of the cloaca to secretory sites along the cloacal orifice. Cladistic analyses indicate that the variation in presence of anterior ventral glands is due to homoplasy. The occurrence of female vent glands, bifurcated dorsal glands, and the pseudopenis supports a phylogeny based upon non-cloacal characters.

Animals↗

Olfactory receptor gene expression in tiger salamander olfactory epithelium.

Physiological studies of odor-elicited responses from the olfactory epithelium and bulb in the tiger salamander, Ambystoma tigrinum, have elucidated a number of features of olfactory coding that appear to be conserved across several vertebrate species. This animal model has provided an accessible in vivo system for observing individual and ensemble olfactory responses to odorant stimulation using biochemical, neurophysiological, and behavioral assays. In this paper we have complemented these studies by characterizing 35 candidate odorant receptor genes. These receptor sequences are similar to those of the large families of olfactory receptors found in mammals and fish. In situ hybridization, using RNA probes to 20 of these sequences, demonstrates differential distributions of labeled cells across the extent and within the depth of the olfactory epithelium. The distributions of cells labeled with probes to different receptors show spatially restricted patterns that are generally localized to different degrees in medial-lateral and anterior-posterior directions. The patterns of receptor expression in the ventral olfactory epithelium (OE) are mirrored in the dorsal OE. We present a hypothesis as to how the sensory neuron populations expressing different receptor types responding to a particular odorant may relate to the distribution patterns of epithelial and bulbar responses previously characterized using single-unit and voltage-sensitive dye recording methods.

Ambystoma↗

Connectivity and cytoarchitecture of the ventral telencephalon in the salamander Plethodon shermani.

The cytoarchitecture and axonal connection pattern of centers in the ventral telencephalon of the salamander Plethodon shermani were studied using biocytin for anterograde and retrograde labeling of cell groups, as well as by intracellular injections. Application of biocytin to the main and accessory olfactory bulbs identified the olfactory pallial regions and the vomeronasal portion of the amygdala, respectively. According to our results, the amygdala of Plethodon is divided into (1) a rostral part projecting to visceral and limbic centers and receiving afferents from the dorsal thalamus, and (2) a caudal part receiving accessory olfactory input. The striatopallial transition area (SPTA) lies rostrodorsally to the caudal (vomeronasal) amygdala and is similar in connections and possibly in function. The rostral striatum has few descending projections to the medulla, whereas the intermediate striatum sends strong projections to the tegmentum and medulla. The caudal striatum has strong ascending projections to the striatum and descending projections to the ventral hypothalamus. The dendritic trees of neurons labeled below the striatum and in the SPTA spread laterally from the soma, whereas dendrites of striatal neurons converge into the laterally situated striatal neuropil. In the caudal amygdala, three distinct types of neurons are found differing in dendritic arborization. It is concluded that, hodologically, the rostral part of the urodele amygdala corresponds to the central and basolateral amygdala and the caudal part to the cortical/medial amygdala of mammals. The urodele striatum is divided into a rostral striatum proper, an intermediate dorsal pallidum, and a caudal part, with distinct connections described here for the first time in a vertebrate.

Animals↗

Distribution of GABA, glycine, and glutamate in neurons of the medulla oblongata and their projections to the midbrain tectum in plethodontid salamanders.

In the medulla oblongata of plethodontid salamanders, GABA-, glycine-, and glutamate-like immunoreactivity (ir) of neurons was studied. Combined tracing and immunohistochemical experiments were performed to analyze the transmitter content of medullary nuclei with reciprocal connections with the tectum mesencephali. The distribution of transmitters differed significantly between rostral and caudal medulla; dual or triple localization of transmitters was present in somata throughout the rostrocaudal extent of the medulla. Regarding the rostral medulla, the largest number of GABA- and gly-ir neurons was found in the medial zone. Neurons of the nucleus reticularis medius (NRM) retrogradely labeled by tracer application into the tectum revealed predominantly gly-ir, often colocalized with glu-ir. The NRM appears to be homologous to the mammalian gigantocellular reticular nucleus, and its glycinergic projection is most likely part of a negative feedback loop between medulla and tectum. Neurons of the dorsal and vestibular nucleus projecting to the tectum were glu-ir and often revealed additional GABA- and/or gly-ir in the vestibular nucleus. Regarding the caudal medulla, the highest density of GABA- and gly-ir cells was found in the lateral zone. Differences in the neurochemistry of the rostral versus caudal medulla appear to result from the transmitter content of projection nuclei in the rostral medulla and support the idea that the rostral medulla is involved in tecto-reticular interaction. Our results likewise underline the role of the NRM in visual object selection and orientation as suggested by behavioral studies and recordings from tectal neurons.

Animals↗

Immunocytochemical analysis of GABA-positive and calretinin-positive horizontal cells in the tiger salamander retina.

By using immunocytochemical techniques, we demonstrate that there are two distinct, nonoverlapping populations of horizontal cells (HCs) in the tiger salamander retina: GABA-positive cells account for about 72% and GABA-negative (calretinin-positive) cells account for 28% of the total HC somas. The calretinin-positive HCs have relatively sparse and thick dendrites: soma diameter of 19.72 +/- 0.29 microm, and soma density of 140 +/- 13 cells/mm(2), morphological features very much like the A-type HCs described in the accompanying article. The GABA-positive HCs have thinner dendritic and coarse axon-terminal-like processes of higher density: soma diameter of 18 +/- 0.18 microm, and soma density of 364 +/- 18 cells/mm(2), features that very much resemble the B-type HCs and B-type HC axon terminals in the accompanying article. By using double and triple immunostaining techniques we found that only 18% of the non-GABAergic HC dendritic clusters contact rods, whereas the remaining 82% of the dendritic clusters contact cones. This is consistent with the physiological finding in the accompanying article that the A-type HCs are cone-dominated. On the other hand, 32% of GABAergic HC dendrites contact rod pedicles and 68% contact cone pedicles, consistent with the physiological finding that B-type HCs and B-type HC axon terminals receive mixed rod/cone inputs. Detailed confocal microscope analysis shows that 4% rods, 6% principal double cones/single cones, and 100% accessory double cones contact calretinin-positive HCs, and 79% rods, 100% principal double cones, 14% accessory double cones, and 82% single cones contact GABAergic HCs. These results suggest that GABAergic and non-GABAergic HC input/output synapses differ and they may mediate different functional pathways in the outer retina.

Ambystoma↗