Retinal ganglion cell morphology in the frog, Rana pipiens

The morphology of retinal ganglion cells in the frog, Rana pipiens, has been examined in retinal flatmounts following backfilling of axons with horseradish peroxidase (HRP). Size and shape of the cell body and of the dendritic arbor, the dendritic branching pattern, and the depth of dendritic arborization within the inner plexiform layer (IPL) were all used to classify these cells. All of the ganglion cells so visualized can be grouped into one of 7 distinct cell classes. Class 1 contains the largest ganglion cells, with a soma size of 323 +/- 5.3 microns2 and dendritic fields of 86,819 +/- 11,817 microns2; the dendrites branch within strata 1 and 2 of the IPL. The second largest cells are class 2, with somas of 245 +/- 19.7 microns2 and dendritic fields of 55,983 +/- 7,392 microns2; the dendrites also branch within strata 1 and 2 of the IPL. Class 3 cells are the next largest class with somas of 211 +/- 11.8 microns2 and dendritic fields of 18,186 +/- 1,394 microns2; there are three varieties of class 3 cells based on the depth of branching of the dendrites: some cells are bistratified, others are tristratified, while still other cells arborize diffusely within the IPL. Class 4 cells are intermediate in size, with somas of 113 +/- 7.4 microns2 and dendrites of 4800 +/- 759 microns2; the dendrites arborize within strata 4 and 5 of the IPL. Class 5 cells have not been quantitatively analyzed because they are heterogeneous in soma and dendritic size. However, class 5 cells all have cell bodies displaced in location into the inner nuclear layer and all have a unique dendritic specialization: they send from 1 to 3 processes into the outer plexiform layer. Class 6 cells are the second smallest cell class with somas of 68.1 +/- 5.13 microns2 and dendritic fields of 888 +/- 182 microns2; the dendrites arborize within strata 3, 4, and 5 of the IP. Class 7 contains the smallest ganglion cells with somas of 62.1 +/- 2.86 microns2 and dendritic fields of 831 +/- 74.2 microns2; the dendrites arborize within strata 3, 4, and 5 of the IPL. The frequency of each cell class is inversely proportional to the size of the dendritic field. Thus, class 7 cells are the most frequent; class 1 cells are the least frequent. Furthermore, each of these 7 classes of ganglion cells has representative cells located in the inner nuclear layer.(ABSTRACT TRUNCATED AT 400 WORDS)     

Pathway-specific maturation, visual deprivation, and development of retinal pathway.

One of the fundamental features of the visual system is the segregation of neural circuits that process increments and decrements of luminance into ON and OFF pathways. In mature retina, the dendrites of retinal ganglion cells (RGCs) in the inner plexiform layer (IPL) of retina are separated into ON or OFF sublamina-specific stratification. At an early developmental stage, however, the dendrites of most RGCs are ramified throughout the IPL. The maturation of RGC ON/OFF dendritic stratification requires neural activities mediated by afferent inputs from bipolar and amacrine cells. The synchronized spontaneous burst activities in early postnatal developing retina regulate RGC dendritic filopodial movements and the maintenance or elimination of dendritic processes. After eye opening, visual experience further remodels and consolidates the retinal neural circuit into mature forms. Several neurotransmitter systems, including glutamatergic, acetylcholinergic, GABAergic, and glycinergic systems, might act together to modulate the RGC dendritic refinement. In addition, both the bipolar cells and cholinergic amacrine cells may provide laminar cues for the maturation of RGC dendritic stratification.     

The development of retinal ganglion cell dendritic stratification in ferrets.

A signature feature of mature ferret retinal ganglion cells (RGCs) is the stratification of their dendrites within either ON or OFF sublayers of the retinal inner plexiform layer (IPL). Dendritic stratification is achieved through the gradual restriction of RGC dendrites which initially ramify throughout the IPL. We examined the time course of stratification by retrogradely labeling ferret retinas with DiI at various postnatal ages. Stratification of beta and alpha RGC dendrites into either the ON or OFF sublayers of the IPL begins around postnatal day 5, when class-specific morphologies begin to emerge, and is largely completed by eye opening, at the end of the first postnatal month. Our results imply that dendritic stratification of ferret ON and OFF RGCs, as in other mammals, occurs independently of visually driven activity.     

Long-term treatment of the developing retina with the metabotropic glutamate agonist APB induces long-term changes in the stratification of retinal ganglion cell dendrites

The gradual restriction of initially multistratified retinal ganglion cell (RGC) dendrites into ON and OFF sublaminae of the inner plexiform layer (IPL) can be effectively blocked by treating the developing retina with 2-amino-4-phosphonobutyrate (APB), the metabotropic glutamate agonist, or by light deprivation. Previous studies have focused on the short-term consequences of such manipulations, so the long-term effects of arresting dendritic stratification on the structural development of RGCs are as yet unknown. In the present study, we have addressed this issue by performing a morphological analysis of alpha RGCs labeled by retrograde transport of horseradish peroxidase injected into the dorsal lateral geniculate nucleus of adult cats that received monocular injections of APB from postnatal (P) day 2 until P30. A large proportion of the alpha cells in the APB-treated eye (44%) were found to have multistratified dendrites that terminated in both the ON and OFF sublaminae of the IPL. The dendritic arborization pattern in the sublaminae of the IPL of these cells was asymmetric, showing a variety of forms. Immunolabeling of retinal cross-sections showed that mGLUR6 receptors appeared normal in density and location, while qualitative observation suggested an increase in the axonal arborization of rod bipolar cells. These findings indicate that long-term treatment of the neonatal retina with APB induces a long- lasting structural reorganization in retinal circuitry that most likely accounts for some of the previously described changes in the functional properties of RGCs.     

Retinal ganglion cell dendrites undergo a visual activity-dependent redistribution after eye opening

Recent studies showed that light stimulation is required for the maturational segregation of retinal ganglion cell (RGC) synaptic connectivity with ON and OFF bipolar cells in mammalian retina. However, it is not clear to what extent light stimulation regulates the maturation of RGC dendritic ramification and synaptic connections. The present work quantitatively analyzed the dendritic ramification patterns of different morphological subtypes of RGCs of developing mouse retinas and demonstrated that RGCs in all four major morphological subtypes underwent profound dendritic redistributions from the center to specific stratum of the IPL after eye opening. Light deprivation preferentially blocked the developmental RGC dendritic redistribution from the center to sublamina a of the IPL. Interestingly, this developmental redistribution of RGC dendrites could not be explained by a simple developmental elimination of "excess" dendrites and, therefore, suggests a possible mechanism that requires both selective dendritic growth and elimination guided by visual activity.     

Glycine receptor-mediated synaptic transmission regulates the maturation of ganglion cell synaptic connectivity

It is well documented that neuronal activity is required for the developmental segregation of retinal ganglion cell (RGC) synaptic connectivity with ON and OFF bipolar cells in mammalian retina. Our recent study showed that light deprivation preferentially blocked the developmental RGC dendritic redistribution from the center to sublamina a of the inner plexiform layer (IPL). To determine whether OFF signals in visual stimulation are required for OFF RGC dendritic development, the light-evoked responses and dendritic stratification patterns of RGCs in Spastic mutant mice, in which the OFF signal transmission in the rod pathway is largely blocked due to a reduction of glycine receptor (GlyR) expression, were quantitatively studied at different ages and rearing conditions. The dendritic distribution in the IPL of these mice was indistinguishable from wildtype controls at the age of postnatal day (P)12. However, the adult Spastic mutants had altered RGC light-evoked synaptic inputs from ON and OFF pathways, which could not be mimicked by pharmacologically blocking of glycinergic synaptic transmission on age-matched wildtype animals. Spastic mutation also blocked the developmental redistribution of RGC dendrites from the center to sublamina a of the IPL, which mimicked the effects induced by light deprivation on wildtype animals. Moreover, light deprivation of the Spastic mutants had no additional impact on the RGC dendritic distribution and light response patterns. We interpret these results as that visual stimulation regulates the maturation of RGC synaptic activity and connectivity primarily through GlyR-mediated synaptic transmission.     

Morphological properties of chick retinal ganglion cells in relation to their central projections

Morphological properties of chick retinal ganglion cells (RGCs) were studied in relation to their central projections in 23 chicks. A total of 217 RGCs were retrogradely labeled by applying a carbocyanine dye (DiI) to the thalamus and optic tectum. The labeled RGCs were classified into six groups on the basis of their somal areas, dendritic fields, and branching patterns. The dendrites of these RGCs extended horizontally in the inner plexiform layer (IPL) forming eight dendritic strata. The RGCs in each group showed certain specificities in their central projections. Group Ic predominantly projected to the tectum. Groups IIs and IIIs showed a high thalamic dominance. Groups Is and IIc were nonspecific with regard to their tectal and thalamic projections. Group IVc showed tectal‐specific projections. Occurrence rates of the dendritic strata increased progressively toward the inner part of the IPL, i.e., DSs (dendritic strata) 1–4 were scantily distributed, DSs 5 and 6 were moderately distributed, and DSs 7 and 8 were the most frequently distributed. A total of 42 dendritic stratification patterns were identified, and of these, 18 patterns were common to the tectal RGCs (tec‐RGCs) and thalamic RGCs (tha‐RGCs). The common patterns were detected very frequently in the tec‐ and tha‐RGCs (≈85%), and the dendritic strata were largely distributed in the inner part of the IPL (DSs 5–8). In contrast, the remaining 24 noncommon stratification patterns showed low occurrence rates (≈15%); however, these dendritic strata were widely distributed in both the outer (DSs 1–4) and inner (DSs 5–8) IPL. J. Comp. Neurol. 514:117–130, 2009. © 2009 Wiley‐Liss, Inc.     

Axon-bearing amacrine cells of the macaque monkey retina

A new and remarkable type of amacrine cell has been identified in the primate retina. Application of the vital dye acridine orange to macaque retinas maintained in vitro produced a stable fluorescence in the somata of apparently all retinal neurons in both the inner nuclear and ganglion cell layers. Large somata (approximately 15-20 microns diam) were also consistently observed in the approximate center of the inner plexiform layer (IPL). Intracellular injections of horseradish peroxidase (HRP) made under direct microscopic control showed that the cells in the middle of the IPL constitute a single, morphologically distinct amacrine cell subpopulation. An unusual and characteristic feature of this cell type is the presence of multiple axons that arise from the dendritic tree and project beyond it to form a second, morphologically distinct arborization within the IPL; these cells have thus been referred to as axon-bearing amacrine cells. The dendritic tree of the axon-bearing amacrine cell is highly branched (approximately 40-50 terminal dendrites) and broadly stratified, spanning the central 50% of the IPL so that the soma is situated between the outermost and innermost branches. Dendritic field size increases from approximately 200 microns in diameter within 2 mm of the fovea to approximately 500 microns in the retinal periphery. HRP injections of groups of neighboring cells revealed a regular intercell spacing (approximately 200-300 microns in the retinal periphery), suggesting that dendritic territories uniformly cover the retina. One to four axons originate from the proximal dendrites as thin (less than 0.5 microns), smooth processes. The axons increase in diameter (approximately 1-2 microns) as they course beyond the dendritic field and bifurcate once or twice into secondary branches. These branches give rise to a number of thin, bouton-bearing collaterals that extend radially from the dendritic tree for 1-3 mm without much further branching. The result is a sparsely branched and widely spreading axonal tree that concentrically surrounds the smaller, more highly branched dendritic tree. The axonal tree is narrowly stratified over the central 10-20% of the IPL; it is approximately ten times the diameter of the dendritic tree, resulting in a 100 times greater coverage factor. The clear division of an amacrine cell's processes into distinct dendritic and axonal components has recently been observed in other, morphologically distinct amacrine cell types of the cat and monkey retina and therefore represents a property common to a number of functionally distinct cell types. It is hypothesized that the axon-bearing amacrine cells, like classical neurons,     

Effects of visual or light deprivation on the morphology, and the elimination of the transient features during development, of type I retinal ganglion cells in hamsters

Intracellular injection of Lucifer Yellow (LY) was used to study the detailed morphology of the normal visually deprived, and light-deprived superior colliculus projecting Type I retinal ganglion cells (RGCs) in hamsters. The soma size of the normal Type I cells ranged from 337 to 583 microns 2 with a mean of 436 microns 2. Two to six primary dendrites were observed in these cells. The mean dendritic field diameter was 495 microns and ranged from 309 to 702 microns. The dendritic field diameter of this population of cells exhibited an eccentricity dependence. Quantitative comparisons between the normal and visually deprived or light-deprived Type I RGCs indicated that the morphology of these three groups of cells were similar to each other in terms of the soma size, dendritic field diameter, branching pattern, and total length of the dendrites. During the normal development of cats and hamsters, several transient features, such as exuberant dendritic spines and intraretinal axonal branches, have been observed in the developing RGCs. The complete elimination of these transient features occurs at about 3 and 2 weeks after the opening of the eyes in cats and hamsters, respectively. In the present study, the hypothesis whether visual experience or light stimulation is required for the elimination of these transient features during development was examined. After studying a total of 115 mature Type I RGCs, which included cells from the normal, visually deprived and light deprived animals, no transient feature was observed. We conclude that visual or light deprivation has no effect on the morphological development of superior colliculus projecting Type I RGCs in hamsters, and the elimination of the transient features on the Type I RGCs during development does not depend on visual experience or light stimulation.     

Laminar distributions of interneurons in the main olfactory bulb of the adult hamster

The laminar distributions of intemeurons in the hamster olfactory bulb were studied with rapid Golgi techniques. Eight morphologically distinct classes of intemeurons were characterized according to their somal locations and their dendritic and axonal properties. Two of these classes, Blanes and Golgi cells, had somata restricted to the deeper layers of the bulb and were not observed more superficially than the mitral body layer (MBL). Their dendrites and axons were predominantly situated within the granule cell layer (GRL) and internal plexiform layer (IPL) but occassionally could be traced as superficially as the deeper portion of the external plexiform layer (EPL). Neither their dendrites nor their axons were oriented consistently with respect to the layers of the bulb. Blanes cells had numerous dendritic spines whereas Golgi cells were relatively spine-poor. Two other classes had somata that were restricted to the IPL and MBL, and had dendrites that exhibited clear orientations with respect to these layers. One class, horizontal cells, had dendrites that ran tangentially within the IPL and MBL. The other class, Cajal cells, had radially oriented dendrites that extended peripherally into the superficial region of the EPL and centrally for greater distances into the GRL. Both classes had axons that projected superficially into the EPL. The granule cells in our material were similar to those described in other species. The sixth class of intemeurons was designated as Van Gehuchten cells. The somata of Van Gehuchten cells were restricted to the EPL and MBL. Their processes branched elaborately within the EPL and MBL but were not oriented consistently with respect to these layers. It is unclear from our material whether these cells bear axons or whether they are amacrine intemeurons. Another class, superficial short axon cells, had somata that were predominantly located at the boundary between the EPL and the glomerular layer (GL) but could also be found throughout the periglomerular region and the superficial half of the EPL. These cells had dendritic and axonal processes that extended predominantly into the GL and appeared to branch around and between individual glomeruli. The eighth class, periglomerular cells, had somata located throughout the GL. Most of these cells gave rise to one dendritic trunk that arborized within a single glomerulus. Occassionally a second, less elaborate dendritic process emerged from the main trunk or from the soma and extended into the periglomerular space or encroached upon an adjacent glomerulus. However, we did not find any periglomerular cells with extensive dendritic arbors in more than one glomerulus. These distributions are discussed in relation to the notion that olfactory bulb interneurons may be assigned to two functional groups associated with two distinct levels of integration.     

Laminar distributions of internuerons in the main olfactory bulb of the adult hamster

The laminar distributions of intemeurons in the hamster olfactory bulb were studied with rapid Golgi techniques. Eight morphologically distinct classes of intemeurons were characterized according to their somal locations and their dendritic and axonal properties. Two of these classes, Blanes and Golgi cells, had somata restricted to the deeper layers of the bulb and were not observed more superficially than the mitral body layer (MBL). Their dendrites and axons were predominantly situated within the granule cell layer (GRL) and internal plexiform layer (IPL) but occassionally could be traced as superficially as the deeper portion of the external plexiform layer (EPL). Neither their dendrites nor their axons were oriented consistently with respect to the layers of the bulb. Blanes cells had numerous dendritic spines whereas Golgi cells were relatively spine-poor. Two other classes had somata that were restricted to the IPL and MBL, and had dendrites that exhibited clear orientations with respect to these layers. One class, horizontal cells, had dendrites that ran tangentially within the IPL and MBL. The other class, Cajal cells, had radially oriented dendrites that extended peripherally into the superficial region of the EPL and centrally for greater distances into the GRL. Both classes had axons that projected superficially into the EPL. The granule cells in our material were similar to those described in other species. The sixth class of intemeurons was designated as Van Gehuchten cells. The somata of Van Gehuchten cells were restricted to the EPL and MBL. Their processes branched elaborately within the EPL and MBL but were not oriented consistently with respect to these layers. It is unclear from our material whether these cells bear axons or whether they are amacrine intemeurons. Another class, superficial short axon cells, had somata that were predominantly located at the boundary between the EPL and the glomerular layer (GL) but could also be found throughout the periglomerular region and the superficial half of the EPL. These cells had dendritic and axonal processes that extended predominantly into the GL and appeared to branch around and between individual glomeruli. The eighth class, periglomerular cells, had somata located throughout the GL. Most of these cells gave rise to one dendritic trunk that arborized within a single glomerulus. Occassionally a second, less elaborate dendritic process emerged from the main trunk or from the soma and extended into the periglomerular space or encroached upon an adjacent glomerulus. However, we did not find any periglomerular cells with extensive dendritic arbors in more than one glomerulus. These distributions are discussed in relation to the notion that olfactory bulb interneurons may be assigned to two functional groups associated with two distinct levels of integration.     

Morphologic analysis and classification of ganglion cells of the chick retina by intracellular injection of Lucifer Yellow and retrograde labeling with DiI

Retinal ganglion cells (RGCs) of chicks were labeled by using the techniques of intracellular filling with Lucifer Yellow and retrograde axonal labeling with carbocyanine dye (DiI). Labeled RGCs were morphologically analyzed and classified into four major groups: Group I cells (57.1%) with a small somal area (77.5 microm(2) on average) and narrow dendritic field (17,160 microm(2) on average), Group II cells (28%) with a middle-sized somal area (186 microm(2)) and middle-sized dendritic field (48,800 microm(2)), Group III cells (9.9%) with a middle-sized somal area (203 microm(2)) and wide dendritic field (114,000 microm(2)), and Group IV cells (5%) with a large somal area (399 microm(2)) and wide dendritic field (117,000 microm(2)). Of the four groups, Groups I and II were further subdivided into two types, simple and complex, on the basis of dendritic arborization: Groups Is, Ic, and Groups IIs, IIc. However, Group III and IV showed either a simple or complex type, Group IIIs and Group IVc, respectively. The density of branching points of dendrites was approximately 10 times higher in the complex types (18,350, 6,190, and 3,520 points/mm(2) in Group Ic, IIc, and IVc, respectively) than in the simple types (1,890, 640, and 480 points/mm(2) in Group Is, IIs, and IIIs). The branching density of Group I cells was extremely high in the central zone. The chick inner plexiform layer was divided into eight sublayers by dendritic strata of RGCs and 26 stratification patterns were discriminated. The central and peripheral retinal zones were characterized by branching density of dendrites and composition of RGC groups, respectively.     

Regulation of neonatal development of retinal ganglion cell dendrites by neurotrophin‐3 overexpression

The morphology of dendrites constrains and reflects the nature of synaptic inputs to neurons. The visual system has served as a useful model to show how visual function is determined by the arborization patterns of neuronal processes. In retina, light ON and light OFF responding ganglion cells selectively elaborate their dendritic arbors in distinct sublamina, where they receive, respectively, inputs from ON and OFF bipolar cells. During neonatal maturation, the bilaminarly distributed dendritic arbors of ON‐OFF retinal ganglion cells (RGCs) are refined to more narrowly localized monolaminar structures characteristic of ON or OFF RGCs. Recently, brain‐derived neurotrophic factor (BDNF) has been shown to regulate this laminar refinement, and to enhance the development of dendritic branches selectively of ON RGCs. Although other related neurotrophins are known to regulate neuronal process formation in the central nervous system, little is known about their action in maturing retina. Here, we report that overexpression of neurotrophin‐3 (NT‐3) in the eye accelerates RGC laminar refinement before eye opening. Furthermore, NT‐3 overexpression increases dendritic branch number but reduces dendritic elongation preferentially in ON‐OFF RGCs, a process that also occurs before eye opening. NT‐3 overexpression does affect dendritic maturation in ON RGCs, but to a much less degree. Taken together, our results suggest that NT‐3 and BDNF exhibit overlapping effects in laminar refinement but distinct RGC‐cell‐type specific effects in shaping dendritic arborization during postnatal development. J. Comp. Neurol. 514:449–458, 2009. © 2009 Wiley‐Liss, Inc.     

A distinctive soma size gradient among catecholaminergic neurones of human retinae

We have examined the soma diameters and distribution of catecholaminergic (CA) cells in human retinae, by using an antibody to tyrosine hydroxylase (TH), the rate limiting enzyme in the production of catecholamines. TH-immunoreactivity was detected in two classes of cells (CA1 and CA2 cells). CA1 cells had relatively large somata (mean diameter 14 microns) located in either the inner nuclear layer (INL) or in the ganglion cell layer and extensive dendrites spreading into the other strata of the inner plexiform layer (IPL). CA2 cells had smaller, weakly labelled somata (mean diameter 9.6 microns) located principally in the inner regions of the INL and weakly labelled dendrites extending into the IPL. The mean density of CA2 cells in the far retinal periphery was approximately 38/mm2. The number of CA1 cells averaged approximately 15,600 per retina, with a mean density of 16/mm2. The density distribution of CA1 cells closely paralleled the distribution of ganglion cells, their density peaking at the foveal rim, with an area of relatively high density extending horizontally from the macula region toward the nasal margin (along the visual streak). A distinctive gradient was detected among the soma diameters of CA1 cells: they were largest in the mid-periphery, in a visual streak-like configuration around the optic disk. This gradient of soma size among CA cells closely corresponds to the density distribution of the rod photoreceptors in human retinae.     

Cytoarchitecture of the tectum mesencephali in salamanders: a Golgi and HRP study.

The tectum mesencephali of salamanders shows a morphology that has long been considered primitive when compared with that of frogs. The alternative hypothesis is that the salamander brain is secondarily simplified. In order to test these two hypotheses, the cytoarchitecture of the tectum and the projections of tectal neurons were studied in 11 species of salamanders. Application of the Golgi method reveals three major morphological types. Type 1 has a very wide dendritic arborization mostly confined to the deep fiber layers, and somata are always located within the most superficial part of the periventricular gray matter. Type 2 possesses a wide to medium-size dendritic arborization. In subtype 2a the somata are located in the uppermost part of the gray, and dendrites always reach the uppermost layer of retinal afferents; in subtype 2b the somata are found in deeper parts of the gray, and dendrites arborize in the deeper layers of retinal afferents; and in subtype 2c the somata are also located in deeper parts, but the wide dendritic arborization is confined to deep fiber layers. Type 3 shows the narrowest dendritic arbors that always reach the upper two tectal fiber layers. The somata are found at any depth of the gray matter. HRP experiments reveal a correlation between morphological differences and the projections of tectal neurons. Type 1- and type 2c-like cells constitute the uncrossed tecto-bulbo-spinal tract, whereas type 1- and type 2a-like cells and migrated large spindle-shaped cells (Salamandra) constitute the crossed tecto-bulbo-spinal tract. Type 3-like neurons project to thalamic, pretectal, and isthmic termination sites. The HRP experiments also demonstrate the existence of two classes of mesencephalic trigeminal cells. A comparison shows that salamanders and frogs possess very similar functional and morphological types of tectal cells. However, tectal cells of salamanders show a "juvenile" morphology, and the number of migrated cells is about 10 times higher in frogs compared to salamanders. Both phenomena are seen as the result of secondary simplification of brain structures in the context of paedomorphosis.     

Large retinal ganglion cells in the channel catfish (Ictalurus punctatus): Three types with distinct dendritic stratification patterns form similar but independent mosaics

Retinal ganglion cells in the channel catfish (Ictalurus punctatus) were retrogradely labelled, and those with the largest somata and thickest primary dendrites were categorized by their levels of dendritic stratification. Three types were found, each forming a mosaic making up ～ 1% of the ganglion cell population. Using a system based on established sublaminar terminology, we call these the alpha-a (α_a), alpha-b (α_b), and alpha-c (α_c) ganglion cell mosaics. Cells of the α_a mosaic had large, sparsely branched trees in sublamina a at 10–30% of the depth of the inner plexiform layer (IPL), sclerad to those of all other large ganglion cells. Some α_a somata were displaced into the IPL or inner nuclear layer (INL) but belonged to the same mosaic as their orthotopic counterparts. Cells of the α_a mosaic had dendrites that branched a little more and arborized in sublamina b at 50–60% of the IPL depth. Many also sent fine branches into sublamina a, and some were fully bistratified in a and b. The α_c cells arborized in the most vitread sublamina, sublamina c, at 80–95% of the IPL depth. The soma areas of the three types in the largest retina studied ranged between 139 μm² and 670 μm² with significant differences in the order α_a > α_c ≥ α_b. Analyses based on nearest-neighbour distance (NND) and on spatial auto- and cross-correlograms showed that each mosaic was statistically regular and independent of the others. Mosaic spacings were similar for each type, giving mean NNDs of 242–279 μm in the largest retina and 153–159 μm in a smaller one. Correspondences between these mosaics, previously defined large ganglion cell types in catfish, and other mosaic-forming large ganglion cells in fish and frogs are discussed along with their implications for neuronal classification, function, development, and evolution. © 1995 Wiley-Liss Inc.     

Independent mosaics of large inner- and outer-stratified ganglion cells in the goldfish retina.

Goldfish retinal ganglion cells were filled with horseradish peroxidase and studied in flatmounts. Two regular mosaics of large neurons with many of the properties of mammalian alpha ganglion cells were found, differing from each other in spacing, size, and dendritic stratification. The existence of biplexiform ganglion cells with additional dendrites in the outer plexiform layer was also confirmed. One of the two alpha-like mosaics consisted of giant ganglion cells with thick primary dendrites and large, sparsely branched dendritic trees in the outer sublamina of the inner plexiform layer (IPL). In fish 55-65 mm long, about 300 formed a tessellated array across each retina. Their somata (mean area 277 +/- 6 microns 2) were displaced to varying degrees into the IPL, neighbours in the mosaic often occupying different levels. Their dendrites ramified in one stratum near the inner nuclear layer, at a mean depth of 70.8 +/- 0.5% of the IPL. The other alpha-like mosaic comprised about 900 large ganglion cells, with slightly smaller somata (mean area 193 +/- 4 microns 2) in the ganglion cell layer. Most of their dendrites lay in a narrow stratum at 41.9 +/- 0.5% of the depth of the IPL. However, deviations (usually into more vitread strata) were common, which was not true for similar cells in the distantly related cichlid fish Oreochromis. Measurements of nearest neighbour distance (NND) for 4 outer and 4 inner mosaics showed that they were at least as regular as the alpha cell mosaics of mammals: the ratio of the mean NND to the standard deviation ranged from 4.03 for the least regular outer mosaic to 6.47 for the most regular inner mosaic. The wide phylogenetic distribution of these paired, regular mosaics points to a fundamental role in vision. The presence of some variability in dendritic stratification even within the exceptionally regular inner-stratified mosaic suggests that classifications based entirely on the detailed morphology of individual neurons may not always correlate well with their primary functional roles. Where possible, neuronal morphology and spatial distribution should be studied together.     

The visual system of the channel catfish (Ictalurus punctatus). I. Retinal ganglion cell morphology

Horseradish peroxidase was applied to lesions in the optic nerve of catfish (Ictalurus punctatus). The retinae were processed to reveal HRP-labelled ganglion cells. The histochemical techniques employed allowed fine details of the dendritic arbor to be resolved. Flat-mounted retinae were examined and the following characteristics were noted in individual ganglion cells: Soma area, shape, and depth; number and diameter of major dendrites; shape, area, and depth(s) within the inner plexiform layer (ipl) of the dendritic arbor; origin of the axon (from the soma or a dendrite). On the basis of these characteristics, eleven classes of ganglion cells were delineated: four classes of giant cells (G1-G4) and seven classes of smaller cells (S1-S7). G1 cells had dendrites arborizing in the most distal sublamina of the ipl. G1 cells in the dorsal retina had nasotemporally elongated dendritic arbors. G2 cells had dendrites in the proximal portion of the ipl. G3 cells were almost completely confined to a band running between the nasal and temporal retinal poles, through the center of the retina. In this location, the cells had dorsoventrally elongated dendritic arbors, which were bistratified in the ipl. G4 cells were displaced into the inner nuclear layer. S1 and S4 cells had axons arising from their somata, and dendrites arborizing in the distal and the proximal ipl, respectively. S2 cells were typified by their unstratified dendritic arbors. Similarly, S3 cells were characterised by their bistratified arbors. S5 cells arborized in the most proximal ipl sublamina. S6 cells were small ganglion cells with their somata lying in the inner nuclear layer. S7 cells tended to have complex dendritic arbors, and their axons arose from dendrites.     

A Golgi study of rat neostriatal neurons: light microscopic analysis

At least two types of large neurons (somatic cross-sectional areas, SA greater than 300 microns2) and five-types of medium neurons (SA between 100 and 300 microns2) were distinguished in Golgi preparations of the adult rat neostriatum. Type I large cells had aspinous somata with long, radiating, sparsely spined dendrites which were sometimes varicose distally, whereas type II large cells had spines on both somatic and dendritic surfaces. Type I medium cells had aspinous somata and proximal dendrites, but their distal dendrites were densely covered with spines. Type II medium cells had somatic spines, and their radiating dendrites were sparsely spined. Other medium cells had no somatic spines: Type III cells had poorly branched and sparsely spined dendrites. Type IV cells had profusely branched, sparsely spined dendrites. Type V cells had radiating and varicose dendrites which could also be sparsely spined. Several small neurons (SA mostly less than 100 microns2) were also found in the rat neostriatum: Some had aspinous soma with sparsely spined dendrites; others had somatic spines. Except for the type II large cells, intrinsic axon collaterals were observed for every type of neuron, indicating that they all had local integrating functions.