Aberrant optic axons in the retinal pigment epithelium during chick and quail visual pathway development

Examination of a large number of retinal pigment epithelia revealed that, in a small proportion, optic axons in chick and quail eyes aberrantly entered the pigment cell layer between embryonic day (E) 7 to E14. The aberrant retinal axons originated from the main stream of retinal fibers in the optic nerve and invaded the pigment layer from various positions of the optic nerve head or fissure by growing along the basal side of the pigment epithelium. The axon bundles grew several millimeters into the epithelial sheet and arborized at the margin of the eye. As shown by electron microscopy the nerve fibers occurred as bundles of three to several hundred axons. They always were located at the basal side of the epithelium, and were enveloped by processes of epithelial cells. Very large bundles of axons, however, displaced the epithelial cells from the basal matrix. These retinal axons contacted the pigment epithelial basal lamina. The basal extracellular matrix from the retinal pigment epithelium was isolated and used as substratum for in vitro cultures of various types of neural explants. The matrix preparations consisted of a sheet of a 50 nm thick basal lamina with a central lamina densa, two laminae rarae, and a 15 micron thick stroma. Axons from avian retina explants, as well as sensory ganglia, grew on the basal lamina side of the pigment cell matrix with the same growth rate and with the same fiber density as on similarly prepared basal laminae from the neural retina. These experiments show that the matrix from the pigment epithelium of the avian eye does not have negative effects on axonal growth and indicate that a basal lamina from a normally non-innervated tissue can provide a favorable matrix for axonal growth.     

Axonal redirection at the dorsoventral intraretinal boundary

Cobaltous-lysine applied to the goldfish optic nerve backfilled retinal ganglion cells and their axons. Confined to the ventronasal and ventrotemporal retina was a small population of retinal ganglion cells whose axons traveled dorsally and parallel to the retinal margin. On reaching the boundary between dorsal and ventral retina, the axons arched, joined radially oriented bundles of axons, and traveled toward the optic disk. Control studies showed that the axons came from retinal ganglion cells rather than from retinopetal cells. The somatic area of retinal ganglion cells (RGCs) with circumferential axons was 30-50 microns, and was similar to that of average ganglion cells. The axons of these cells coursed between the optic fiber and ganglion cell layers or between the ganglion cell and inner plexiform layers. Many somata were displaced slightly toward the inner plexiform layer, but were not really displaced ganglion cells. The aberrant axonal trajectory may be related to the slightly displaced location of the cell. However, ganglion cells that are displaced to the edge of the inner nuclear layer usually have radially coursing axons. We digitized the coordinates of the bending points and the dorsoventral retinal boundary. On average, the bending points occurred within 100 microns of the dorsoventral retinal border. These findings suggest that some molecular, rather than mechanical, factor at the dorsoventral retinal boundary alters the course of the circumferential axons. Furthermore, because there are cells with circumferential axons throughout the ventral retina, the data imply that at least ventral RGC axons avoid mingling with the axons from dorsal RGCs.     

The organization of the fibers in the optic nerve of normal and tectum-less Rana pipiens

We have examined the detailed order of retinal ganglion cell (RGC) axons in the optic nerve and tract of the frog, Ranapipiens. By using horseradish peroxidase (HRP) injections into small regions of theretina, the tectum, and at various points along the visual pathway, it hasbeen possible to follow labelled fibers throughout their course in the nerve and tract. Several surprising features in the order of fibers in the visual pathway were discovered in our investigation. The fascicular pattern of RGC axons in che retina is similar to that described in other vertebrates; however, immediately central to their entry into the optic nerve head, approximately half of the fibers from the nasal or temporal retina cross over to the opposite side of the nerve. Although the axons from the dorsal and ventral regions of the retina generally remain in the dorsal and ventral regions of the nerve, some fiber crossing occurs in those axons as well. The result of this seemingly complex rearrangement is that the optic nerve of Rana pipiens contains mirror symmetric representations of the retinal surface on either side of the dorsal ventral midline of the nerve. The fibers in each of these representation are arranged as semicircles representing the full circumference of the retina. This precise fiber order is preserved in the nerve until immediately periphearal to the optic chiasm, at which point age-related axon from both side of the nerve bundle together. Consequently, when a small pellet of HRP is placed in the chiasmic region of the nerve, an annualus of retinal ganglion cells and a corresponding annulus of RGC terminals in the tectum are la belled. As the age-related bundles of fibers emerge from the chiasm they split to form a medial bundle and a lateral bundle, which grow in the medial and lateral branches of the optic tract, respectively. Although the course followed by RGC axons in the visual pathv/ay is complex, we propose a model in which the organization of fibers in the nerve and tract can arise from a few rules of axon guidance. To determine whether the optic tecta, the primary retinal targets, play a role in the development and organization of the optic nerve and tract, we removed the tectal primordia in Rana embryos and examined the order in the nerve when the animals had reached larval stages. We found that the order in the nerve and tract was well preserved in tectumless frogs. Therefore, we propose that guidance factors independent of the target direct axon growth in the frog visual system.     

Visual system of the channel catfish (Ictalurus punctatus): III. Fiber order in the optic nerve and optic tract

In channel catfish the ganglion cell axons leave the retina via a ring of approximately 13 separate optic papillae. Each papilla serves an area of retina extending from the central zone of the retina to the periphery. Papillae located at a dorsal position in the ring serve exclusively dorsal retina. Ventrally located papillae, however, have an exaggerated peripheral retinal representation, so that they serve mostly ventral retina but also some areas of peripheral retina dorsal to the nasal and temporal poles. The ganglion cell axon bundles departing from the retina via individual papillae were labelled with horseradish peroxidase, and sections of the optic pathway were examined to reveal the topographic organization of the fibers. The topographic order of the optic nerve was dissimilar to that of cichlids and goldfish. Fibers from individual papillae remained together throughout the optic nerve. Close to the optic nerve head, the papillae were arranged as a continuum around the U-shaped optic nerve, without the discontinuity in the representation of the ventral retina seen in other fish. Fibers associated with the dorsal papillae were located at the tip of the caudolateral arm of the U, and fibers from ventral papillae were on the rostromedial arm. Fibers from nasally and temporally located papillae were found on the base of the U. By the level of the optic chiasm the U shape had flattened out but retained the relative ordering of the papillae. Rotation of the nerve as it became the optic tract brought the representation of the ventral papillae to the dorsal pole of the tract, and the dorsal papillae to the ventral tract. It was only in the optic tract that rearrangement of fibers became apparent. As described above, the axons of some ganglion cells in dorsal, peripheral retina left the retina and travelled through the optic nerve with axons from extreme ventral retina. In the optic tract, these dorsal fibers joined the main body of fibers from the dorsal retina. The significance of these observations for theories of fiber rearrangement is discussed.     

Cross-species collapse activity of polarized radial glia on retinal ganglion cell axons

Inhibition of incorrect axonal outgrowth has been shown to be a crucial guidance mechanism during the development of the nervous system. Within the visual system of chick and rat, extension of retinal ganglion cell axons is essentially restricted to distinct layers of the retina and distinct brain regions such as the tectum opticum. In addition, populations of ganglion cells from defined retina locations project topographically to defined tectal areas, their growth possibly being inhibited by radial glia in incorrect tectal regions. In the current study, we aimed to analyse potential inhibitory activity of retinal glia during outgrowth of ganglion cell axons of embryonic chick and rat. The response of ganglion cell axons originating from different retina locations when exposed to purified retinal radial glia cell membranes were monitored in collapse assays by time lapse video recording. The interaction of axons growing on purified glial somata or glial endfeet was analysed in outgrowth assays. Our results indicate that (1) nasal and temporal chick growth cones are equally induced to collapse by cell membranes from retinal radial glia: 75% nasal and 72% temporal. (2) The collapse inducing component of radial glia can be inactivated by defined heat treatment, reducing collapsing activity to 6% nasal and 5% temporal. (3) Rat growth cones respond in a similar way to chick radial glia. (4) Rat axons grow perfectly on endfeet but not on somata of radial glia of the chick. In summary, the data suggest that radial glia are functionally polarized with permissive endfeet and inhibitory somata based on heat-labile proteins. Glia polarization is likely to inhibit aberrant growth of ganglion cell axons into outer retina layers. However, retinal radial glia are unlikely to participate in preordering axons within the retina and therefore do not affect the topographic projection. Finally, the inhibitory function of radial glia is conserved between birds and mammals and represents possibly a fundamental mechanism for structuring the central nervous system. GLIA 25:143–153, 1999. © 1999 Wiley-Liss, Inc.     

Distribution and morphology of retinal ganglion cells in the Japanese quail

A ganglion cell density map was produced from the Nissl-stained retinal whole mount of the Japanese quail. Ganglion cell density diminished nearly concentrically from the central area toward the retinal periphery. The mean soma area of ganglion cells in isodensity zones increased as the cell density decreased. The histograms of soma areas in each zone indicated that a population of small-sized ganglion cells persists into the peripheral retina. The total number of ganglion cells was estimated at about 2.0 million. Electron microscopic examination of the optic nerve revealed thin unmyelinated axons to comprise 69% of the total fiber count (about 2.0 million). Since there was no discrepancy between both the total numbers of neurons in the ganglion cell layer and optic nerve fibers, it is inferred that displaced amacrine cells are few, if any. The spectrum in optic nerve fiber diameter showed a unimodal skewed distribution quite similar to the histogram of soma areas of ganglion cells in the whole retina. This suggests a close correlation between soma areas and axon diameters. Retinal ganglion cells filled from the optic nerve with horseradish peroxidase were classified into 7 types according to such morphological characteristics as size, shape and location of the soma, as well as dendritic arborization pattern. Taking into account areal ranges of somata of each cell type, it can be assumed that most of the ganglion cells in the whole retinal ganglion cell layer are composed of type I, II and III cells, and that the population of uniformly small-sized ganglion cells corresponds to type I cells and is an origin of unmyelinated axons in the optic nerve.     

Will central nervous systems in the adult mammal regenerate after bypassing a lesion? A study in the mouse and chick visual systems

We determined whether or not optic axons in the adult mammalian retina would regenerate well if allowed to bypass a lesion scar. In one series we produced microlesions with fine needles in the ganglion cell fiber layer of adult mouse retinas and later examined the retinas as silver-stained flat mounts to observe the behavior of optic axons that bypassed the lesion. Such axons continued to grow abortively, i.e., grew randomly and for only short distances, whether growing within a sector of Wallerian (anterograde) degeneration or in the neighboring zone of intact optic axon bundles. In a second series we produced optic nerve crushes in adult mice and observed the behavior of optic axons growing retrograde into the retina. These fibers similarly grew abortively whether in a zone of intact fiber bundles or when a retinal lesion was produced with the crush, in the sector of Wallerian degeneration. Retinal lesions in newly hatched chicks produced a comparable picture of abortive (short-distance) growth, but the optic and centrifugal fibers had a greater tendency to remain oriented within the ganglion cell fiber layer than did mouse axons. This improved orientation may be the consequence of the greater number of optic fibers in the chick retina and hence the greater opportunity for nonspecific contact guidance. The results indicate that blockage (by a lesion scar or myelin debris) and hypoxia are not the key causes of regenerative failure, as regeneration failed even when those factors were minimal.     

Chiasmatic course of temporal retinal axons in the developing ferret

Recent studies on the distribution of optic axons in the mature visual pathways, as well as on the genesis of their ganglion cells of origin, suggest that the time of axonal arrival at the optic chiasm determines the side of the brain to which a temporal retinal axon will project. The present study has examined this issue directly in fetal ferrets, by determining the projection of the temporal retina at different developmental stages. Fetuses of known gestational age were fixed with paraformaldehyde and subsequently implanted with crystals of the carbocyanine dye, DiI, into eithe the temporal retina, or into one optic tract. The lipophilic diffusion of the dye within the plasma membrane of the axons revealed the course of temporal retinal fibers through the fetal chiasm, as well as the distribution of ganglion cells across the two retinae projecting to one optic tract. During early fetal stages, the temporal retina extends axons preferentially into the ipsilateral optic tract: the early retinal projection shows a classical partial decussation pattern. During later fetal stages, temporal retinal axons can be traced into both optic tracts, and the distribution of cells with crossed and uncrossed optic axons in the temporal retina is overlapping. These results indicate that the mature decussation patterns of retinal ganglion cell classes are not primarily the consequence of regressive phenomena such as cell death; rather, they are formed as axons navigate the chiasmatic region during development. The differences in decussation pattern between cell classes arise from the fact that the mechanisms producing the segregation of nasal and temporal retinal axons at the chiasm must change as development proceeds.     

Intraretinal pathfinding of ganglion cell axons is perturbed by a monoclonal antibody specific for a G4/Ng-CAM-like cell adhesion molecule.

To identify molecular components involved in directed axonal outgrowth and in neural pattern formation, hybridoma technology was employed using the visual system of the chicken as a model system. Using cell surface protein fractions as immunogens, we obtained the monoclonal antibody mAb C4, which binds to a 135 kDa cell surface glycoprotein of the high-mannose or complex type. Within the retina, the C4 antigen is found exclusively in the optic fiber layer. Immuno-double labeling of retinal whole mounts with a glial marker and mAb C4 suggests that the C4 antigen is restricted to ganglion cell axons but not found on Müller glial endfeet. Biochemical and histological data reveal similarities between the C4-antigen and G4/NgCAM. Addition of mAb C4 to retina explants cultured on a striped carpet of tectal cell membranes leads to defasciculation of outgrowing axons, suggesting that the C4 antigen serves as an axon cell adhesion molecule (Ax-CAM). Axon elongation on neighboring axons can be also inhibited by the application of mAb C4 to embryonic retina whole mounts in vitro. The aberrant axon growth into incorrect retina layers observed under these conditions suggests that the C4 antigen functions as a guiding cue for the generation of the retinal optic fiber layer.     

Quantitative analysis of the retinal ganglion cell layer and optic nerve of the barn owl Tyto alba

The visual capacity of the common barn owl (Tyto alba) was studied by quantitative analysis of the retina and optic nerve. Cell counts in the ganglion cell layer of the whole-mounted retina revealed a temporal area centralis with peak cell density of 12,500 cells/mm2 and a horizontal streak of high cell density extending from the area centralis into the nasal retina. Integration of the ganglion cell density map gave an estimated total of 1.4 million cells for the ganglion cell layer. Electron microscopy of a single, complete section of the optic nerve revealed a bimodal fiber diameter spectrum (modes at 0.3 and 0.9 microns; bin width = 0.2 microns), with diameters ranging from 0.15 microns (unmyelinated) to 6.05 microns (myelinated, sheath included). The total axon count for the optic nerve was estimated from sample counts to be about 680,000 axons (25% unmyelinated). Therefore, roughly half of the cells in the retinal ganglion cell layer do not send axons into the optic nerve. With certain assumptions, the data predict a visual spatial acuity for barn owls on the order of 8 cycles/degree, a value similar to the known behaviorally measured acuities of masked owls (10 cycles/degree) and domestic cats (6 cycles/degree).     

Different cell surface areas of polarized radial glia having opposite effects on axonal outgrowth

During neuronal development neurites are likely to be specifically guided to their targets. Within the chicken retina, ganglion cell axons are extended exclusively into the optic fibre layer, but not into the outer retina. We investigated, whether radial glial cells having endfeet at the optic fibre layer and somata in the outer retina, might be involved in neurite guidance. In order to analyse distinct cell surface areas, endfeet and somata of these glial cells were purified. Glial endfeet were isolated from flat mounted retina by a specific detachment procedure. Glial somata were purified by negative selection using a monoclonal antibody/complement mediated cytolysis of all non-glial cells. Retinal tissue strips were explanted either onto pure glial endfeet or onto glial somata. As revealed by scanning and fluorescence microscopy, essentially no ganglion cell axons were evident on glial somata, whereas axonal outgrowth was abundant on glial endfeet. However, when glial somata were heat treated and employed thereafter as the substratum, axon extension was significantly increased. Time-lapse video recording studies indicated that purified cell membranes of glial somata but not of endfeet induced collapse of growth cones. Collapsing activity was destroyed by heat treatment of glial membranes. The collapsing activity of retinal glia was found to be specific for retinal ganglion cell neurites, because growth cones from dorsal root ganglia remained unaffected. Employing four different kinase inhibitors revealed that the investigated protein kinase types were unlikely to be involved in the collapse reaction. The data show for the first time that radial glial cells are functionally polarized having permissive endfeet and inhibitory somata with regard to outgrowing axons. This finding underscores the pivotal role of radial glia in structuring developing nervous systems.     

Disruption of the retinal basal lamina during early embryonic development leads to a retraction of vitreal end feet,an increased number of ganglion cells,and aberrant axonal outgrowth

Bacterial collagenase was injected into the vitreous of the eye of chick and quail embryos. Immunocytochemical and ultrastructural studies revealed that the collagenase dissolved the retinal basal lamina of the injected eye. The basal lamina disruption was first detectable 1 hour after enzyme injection and was complete within 3 hours. With further development, the retinal basal lamina was not reestablished; newly developing neuroepithelium in the peripheral retina, however, generated an intact basal lamina. Western blot analysis showed that Clostridial collagenase degraded various collagens but spared noncollagenous proteins. Basal lamina disruption of embryonic day 3 to 6 retinae led to the retraction of the end feet of the neuroepithelial cells, caused an increase in the number of Islet-1⁺ cells (most likely ganglion cells), an increase in the thickness of the optic fiber layer, and aberrant growth of optic axons on their way toward the optic disc. None of these changes were observed when retinal basal laminae were disrupted at later stages of development. The present data demonstrate that the retinal basal lamina, by anchoring the neuroepithelial cells to the pial surface of the retina, has an important function in the development of the normal cytoarchitecture of this structure. It is proposed that the altered extracellular environment in the vitreal part of the retina, resulting in the retraction of the neuroepithelial end feet, is responsible for the increased number of Islet-1⁺ cells and the aberrant axonal navigation. J. Comp. Neurol. 397:89–104, 1998. © 1998 Wiley-Liss, Inc.     

Factors guiding optic fibers in developing Xenopus retina

We have characterized, by electron microscopy, the growth of pioneering axons from the retina into the visual pathway during early development of Xenopus laevis. The subsequent development of following fibers from the growing retinal margin as they accumulated in the ganglion cell fiber layer (GCFL) of the retina was also studied. Extracellular channels bordered by neuroepithelial cells appear in the developing retina in a dorsal to ventral gradient before any pioneering axons are seen. Pioneering axons are subsequently observed in these channels, usually surrounded by neuroepithelial cell processes. Ruthenium red treatment of embryonic retinas reveals extracellular matrix (ECM) within these retinal channels, while extracellular spaces in the proximal optic stalk, just beyond the optic disc, lack this material. ECM is also seen in optic tectum wherever ingrowing retinal and nonretinal axons are found. The channels and the ECM contained within them may provide guidance cues for pioneering retinal axons. The early association of pioneering retinal axons with neuroepithelial cell processes (putative glia) appears to be important in further development of the GCFL. The so-called following fibers of ganglion cells, arising later in development, fasciculate with pioneer axons in extracellular spaces and form fiber bundles of the GCFL on top of the layer of glial cell endfeet. It is not clear whether pioneering axons, glial cell surfaces, or both serve as guidance cues for following fiber migration.     

FGF-2 modulates expression and distribution of GAP-43 in frog retinal ganglion cells after optic nerve injury

Basic fibroblast growth factor (bFGF or FGF-2) has been implicated as a trophic factor that promotes survival and neurite outgrowth of neurons. We found previously that application of FGF-2 to the proximal stump of the injured axon increases retinal ganglion cell (RGC) survival. We determine here the effect of FGF-2 on expression of the axonal growth-associated phosphoprotein (GAP)-43 in retinal ganglion cells and tectum of Rana pipiens during regeneration of the optic nerve. In control retinas, GAP-43 protein was found in the optic fiber layer and in optic nerve; mRNA levels were low. After axotomy, mRNA levels increased sevenfold and GAP-43 protein was significantly increased. GAP-43 was localized in retinal axons and in a subset of RGC cell bodies and dendrites. This upregulation of GAP-43 was sustained through the period in which retinal axons reconnect with their target in the tectum. FGF-2 application to the injured nerve, but not to the eyeball, increased GAP-43 mRNA in the retina but decreased GAP-43 protein levels and decreased the number of immunopositive cell bodies. In the tectum, no treatment affected GAP-43 mRNA but FGF-2 application to the axotomized optic nerve increased GAP-43 protein in regenerating retinal projections. We conclude that FGF-2 upregulates the synthesis and alters the distribution of the axonal growth-promoting protein GAP-43, suggesting that it may enhance axonal regrowth.     

Aberrant axon growth of the chick embryo retina during normal development

Axon growth behavior in the optic nerve was examined using a carbocyanine dye, DiI, as a tracer, DiI facilitated clear visualization of the whole growth pattern of the optic nerve, i.e. the initial association of axons, fasciculated growth within the optic fiber layer and flattened growth cones in both living and fixed chick embryo retinae. Retrograde labelling with DiI in fixed retinae revealed that a considerable number of ganglion cells were apparently misdirected, extending their axons toward the periphery of the retina during normal development. The maximum proportion of aberrant ganglion cells reached about 15% of the total upon staining with a single DiI crystal. Misdirection was predominantly observed in retinae prepared from 6- to 8-day-old chick embryos. In embryos more than 9 days old, however, distinction of aberrant ganglion cells from normal ones became difficult, so that any degeneration of misdirected ganglion cells could not be clarified. Almost all of the misdirected ganglion cells were oriented centrifugally to the retinal periphery. These results indicate that misdirection occurs spontaneously during normal development even within the retina.     

Localization and Synaptic Release of N-acetylaspartylglutamate in the Chick Retina and Optic Tectum

The neuropeptide, N-acetylaspartylglutamate (NAAG), was identified in the chick retina (1.4 nmol/retina) by HPLC, radioimmunoassay and immunohistochemistry. This acidic dipeptide was found within retinal ganglion cell bodies and their neurites in the optic fibre layer of the retina. Substantial, but less intense, immunoreactivity was detected in many amacrine-like cells in the inner nuclear layer and in multiple bands within the inner plexiform layer. In addition, NAAG immunoreactivity was observed in the optic fibre layer and in the neuropil of the superficial layers of the optic tectum, as well as in many cell bodies in the tectum. Using a newly developed, specific and highly sensitive (3 fmol/50 microl) radioimmunoassay for NAAG, peptide release was detected in isolated retinas upon depolarization with 55 mM extracellular potassium. This assay also permitted detection of peptide release from the optic tectum following stimulation of action potentials in retinal ganglion cell axons of the optic tract. Both of these release processes required the presence of extracellular calcium. Electrically stimulated release from the tectum was reversibly blocked by extracellular cadmium. These findings suggest that NAAG serves an extracellular function following depolarization-induced release from retinal amacrine neurons and from ganglion cell axon endings in the chick optic tectum. These data support the hypothesis that NAAG functions in synaptic communication between neurons in the visual system.     

Increased brain size and glial cell number in CD81-null mice

Retinal axons undergo several changes in organization as they pass through the region of the optic chiasm and optic tract. We used immunocytochemistry to examine the possible involvement of fibroblast growth factor receptors (FGFR) in these changes in retinal axon growth. In the retina, at all ages examined, prominent staining for FGFR was seen in the optic fiber layer and at the optic disk. At embryonic day 15 (E15), FGFR immunoreactivity was also detected in the ganglion cell layer, as defined by immunoreactivity for islet-1. At later developmental stages (E16 to postnatal day 0), FGFR were found in the optic fiber layer and the inner plexiform layer. In the ventral diencephalon, immunostaining for FGFR was first detected at E13 in a group of cells posterior to the chiasm. These cells appeared to match the neurons that are immunopositive for the stage-specific embryonic antigen-1 (SSEA-1). FGFR staining was also found on the retinal axons at E13. At E14-E16, when most axons are growing across the chiasm and the tract, a dynamic pattern of FGFR immunoreactivity was observed on the retinal axons. The staining was reduced when axons reached the midline but was increased when axons reached the threshold of the optic tract. These results suggest that axon growth and fiber patterning in distinct regions of the retinofugal pathway are in part controlled by a regulated expression of FGFR. Furthermore, the axons with elevated FGFR expression in the optic tract have a posterior border of rich FGFR expression in the lateral part of the diencephalon. This region overlaps with a lateral extension of the SSEA-1-positive cells, suggesting a possible relation of these cells to the elevated expression of FGFR.     

Topography of the retinal projection to the superficial pretectal parvicellular nucleus of goldfish: a cobaltous-lysine study

The retinal projection to the superficial pretectal parvicellular nucleus (SPp) of goldfish was examined by filling select groups of optic axons with cobaltous-lysine. The tracer was applied intraocularly to peripheral retinal slits in some fish. In other fish, it was applied to optic axons from an intact hemiretina after one-half of the retina was ablated and the corresponding optic axons had degenerated. The results indicated that SPp is a folded structure, having a dorsal surface innervated by axons from temporal retinal ganglion cells and a ventral surface innervated by axons from nasal retinal ganglion cells. Peripheral retina innervates the anterodorsal and anteroventral edges of SPp, while central retina innervates the posterior genu. Dorsal retina innervates lateral SPp and ventral retina innervates medial SPp. Thus, although SPp is a folded nucleus, the topography of the retino-SPp projection is similar to the topography of the retinotectal projection. That is, the relative position of optic axons within SPp mirrors the retinal location of the ganglion cells that project to SPp. Retino-SPp axons occupy the center of the main optic tract before it divides into the two optic brachia. These axons are topographically arranged, with temporal retino-SPp axons being flanked on both sides by nasal retino-SPp axons. Retino-SPp axons arborize within SPp and then continue to enter the superficial tectal retino-recipient lamina. Thus, these axons innervate both SPp and the optic tectum. These findings are discussed with respect to chemospecific and morphogenetic views of visual system topography.     

The course of axons of retinal ganglion cells within the optic nerve and tract of the chick (Gallus gallus)

Small laser lesions placed in the posthatch chicken retina resulted in axotomy and then death of all ganglion cells located in a sector peripheral to the primary damage. With the use of silver techniques, the patterns of degenerating retinal fibers in the optic nerve, chiasm, and optic tract were examined. In the proximal part of the optic nerve, radial retinal lesions resulted in a sheet of degenerating axons along the rostrocaudal extent of the nerve. The position of degenerating axons was related to the site of their entry in the optic nerve head with an overlapping distribution of degenerating fibers entering the optic nerve head from equivalent points from the temporal and nasal sides. In the optic chiasm, the distribution of fibers was similar to that seen in the proximal part of the optic nerve. In the optic tract there was a similar mixing of fibers from opposite sides of the retina. The ventral, nasal and temporal retinal fibers lay in the superficial part of the tract whereas the fibers from the nasal and temporal dorsal retina ran in the deeper, medial aspect of the tract. The central-to-peripheral axes of the retina were mapped along the rostrocaudal axis of the tract. As the tract approached the tectum degenerating fibers from single retinal lesions did not always remain together. In the case of a lesion in the ventral nasal retina, degenerating fibers split into two bundles located at opposite ends of the tract only to reunite at their terminal regional at the caudal pole of the tectum.(ABSTRACT TRUNCATED AT 250 WORDS)     

A quantitative study of the relative contribution of different retinal sectors to the innervation of various thalamic and pretectal nuclei in goldfish

The contribution of retinal ganglion cells situated in different retinal quadrants to the innervation of eight nontectal, retinorecipient targets was examined in goldfish. In some fish, cobaltous-lysine was used to selectively fill severed intraretinal ganglion cell axons and the number of filled axons within each nucleus was determined. In other fish, either the dorsal or ventral or nasal or temporal retina was ablated and the remaining axons from the intact retina were filled with cobalt. The density of the cobalt-filled axons within the retinorecipient targets was quantified with a microdensitometer. All of the eight targets received different degrees of innervation when the contributions from dorsal and ventral retina were compared. The suprachiasmatic nucleus received axons from ventral, but not from dorsal, retinal ganglion cells (RGCs), while the nucleus opticus dorsolateralis, nucleus opticus commissurae posterior, and nucleus opticus pretectalis dorsalis received more axons from ventral than from dorsal RGCs. The tuberal region, nucleus corticalis, and the accessory optic nucleus received axons from dorsal, but not from ventral, RGCs. The nucleus opticus pretectalis ventralis received more axons from dorsal then from ventral RGCs. Only one target, nucleus corticalis, appeared to receive more axons from nasal than from temporal RGCs. In general, those nuclei that were closest to the dorsal optic tract were innervated exclusively or predominantly by ventral RGC axons, whereas those nuclei that were closest to the ventral optic tract were innervated exclusively or predominantly by dorsal RGC axons. These data indicate that in this particular vertebrate, the dorsal and ventral retinal regions are not homogeneous with respect to their projections to nontectal nuclei. The possible role that the nontectal nuclei play in determining the course of optic axons is discussed.