Initial disorder and secondary retinotopic refinement of regenerating axons in the optic tract of the goldfish: signs of a new role for axon collateral loss

Development ◽  
1987 ◽  
Vol 101 (2) ◽  
pp. 323-337
Author(s):  
D.L. Becker ◽  
J.E. Cook
Keyword(s):  
Ganglion Cells ◽  
Optic Tract ◽  
Sibling Rivalry ◽  
Axonal Guidance ◽  
Axon Collateral ◽  
Retrograde Labelling ◽  
Average Proportion ◽  
Optic Axons ◽  
Normal Fish ◽  
Dorsal Retina

The optic tract of the goldfish splits into two brachia just before it reaches the tectum, normal optic axons being distributed systematically between the two according to their retinal origins. The orderliness of this division, like that of the retinotectal projection itself, is conventionally attributed to a system of specific axonal guidance cues. However, the brachial distribution of regenerated axons is much less orderly; and, since there is evidence that these axons have many collateral branches in the nerve and tract, the gross order that remains after regeneration could potentially arise secondarily, in parallel with refinement of the retinotectal map, by a preferential loss of collaterals from the inappropriate brachium. The brachial paths of normal axons, and axons regenerated after optic nerve cut for periods ranging from 19 days to 5 years, were therefore studied by anterograde labelling with horseradish peroxidase from discrete retinal lesions or retrograde labelling of ganglion cells from a cut brachium. From 19 to 28 days, regenerating axons showed little or no preference for their normal brachium. During this period (which includes the first week of tectal synaptogenesis) an average of 46á3% of cells retrogradely labelled from a cut medial brachium were in dorsal retina, compared with only 1á45% in normal fish. Some preference for the normal brachium was evident at 35 days and significant order had returned by 42–70 days, when the average proportion of labelled cells in dorsal retina had fallen to 25á4% though the average number in the whole retina was unchanged. Thus a brachial refinement had occurred in parallel with refinement of the retinotectal map. These results support the idea of a selective loss of axon collaterals from the inappropriate brachium, though they do not exclude the possibility of some concurrent gain in the appropriate one. We suggest that refinement may depend on a process we term ‘sibling rivalry’: competition between different collaterals of the same axon to form a critical number of stable tectal synapses, in which the most- normally-routed branches have the best chance of succeeding and surviving. Developing normal axons might also make use of collateral formation and ‘sibling rivalry’ to generate and refine the complex interwoven patterns of the normal optic tract.

Divergent axon collaterals in the regenerating goldfish optic tract: a fluorescence double-label study

Development ◽  
1988 ◽  
Vol 104 (2) ◽  
pp. 317-320
Author(s):  
D.L. Becker ◽  
J.E. Cook
Keyword(s):  
Fluorescent Dyes ◽  
Ganglion Cells ◽  
Optic Tract ◽  
Axon Collaterals ◽  
Retinal Region ◽  
Double Label ◽  
Subsequent Loss ◽  
Optic Axons ◽  
Diamidino Yellow ◽  
Normal Fish

In the normal goldfish, optic axons are distributed between the two arms (brachia) of each optic tract, in such a way that each axon enters the tectum close to its retinotopic termination site. We have shown previously that regenerating axons at first express little or no preference for their normal brachium. Later, however, a partial refinement of the brachial pathway takes place, implying that some axons must have sent out divergent collateral branches and then eliminated the least appropriate. We have now studied the formation and subsequent loss of axon collaterals in regeneration using retrogradely transported fluorescent dyes. We labelled the axons in the medial brachium with Fast Blue and those in the lateral brachium with Diamidino Yellow in a way that avoided cross-contamination. In normal fish, yellow-labelled ganglion cells dominated the dorsal retina and blue-labelled ganglion cells the ventral, with only a narrow zone of overlap. Double-labelled cells were not found. In fish labelled early in regeneration, however, both dyes were spread over the entire retina in single- and double-labelled ganglion cells. As regeneration progressed, each dye again came to dominate its appropriate retinal region; but much less strongly, confirming previous results. At the same time, double-labelled cells became harder to find. From 60 days after nerve cut onwards they were rare, and largely confined to the boundary zone between dorsal and ventral retina.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Multiple phosphorylated variants of the high molecular mass subunit of neurofilaments in axons of retinal cell neurons: characterization and evidence for their differential association with stationary and moving neurofilaments.

1988 ◽  
Vol 107 (6) ◽  
pp. 2689-2701 ◽  
Author(s):  
S E Lewis ◽  
R A Nixon
Keyword(s):  
Molecular Mass ◽  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Optic Tract ◽  
Axoplasmic Transport ◽  
Retinal Cell ◽  
Retinal Ganglion ◽  
Optic Axons ◽  
Single Polypeptide

The 200-kD subunit of neurofilaments (NF-H) functions as a cross-bridge between neurofilaments and the neuronal cytoskeleton. In this study, four phosphorylated NF-H variants were identified as major constituents of axons from a single neuron type, the retinal ganglion cell, and were shown to have characteristics with different functional implications. We resolved four major Coomassie Blue-stained proteins with apparent molecular masses of 197, 200, 205, and 210 kD on high resolution one-dimensional SDS-polyacrylamide gels of mouse optic axons (optic nerve and optic tract). Proteins with the same electrophoretic mobilities were radiolabeled within retinal ganglion cells in vivo after injecting mice intravitreally with [35S]methionine or [3H]proline. Extraction of the radiolabeled protein fraction with 1% Triton X-100 distinguished four insoluble polypeptides (P197, P200, P205, P210) with expected characteristics of NF-H from two soluble neuronal polypeptides (S197, S200) with few properties of neurofilament proteins. The four Triton-insoluble polypeptides displayed greater than 90% structural homology by two-dimensional alpha-chymotryptic iodopeptide map analysis and cross-reacted with four different monoclonal and polyclonal antibodies to NF-H by immunoblot analysis. Each of these four polypeptides advanced along axons primarily in the Group V (SCa) phase of axoplasmic transport. By contrast, the two Triton-soluble polypeptides displayed only a minor degree of alpha-chymotryptic peptide homology with the Triton-insoluble NF-H forms, did not cross-react with NF-H antibodies, and moved primarily in the Group IV (SCb) wave of axoplasmic transport. The four NF-H variants were generated by phosphorylation of a single polypeptide. Each of these polypeptides incorporated 32P when retinal ganglion cells were radiolabeled in vivo with [32P]orthophosphate and each cross-reacted with monoclonal antibodies specifically directed against phosphorylated epitopes on NF-H. When dephosphorylated in vitro with alkaline phosphatase, the four variants disappeared, giving rise to a single polypeptide with the same apparent molecular mass (160 kD) as newly synthesized, unmodified NF-H. The NF-H variants distributed differently along optic axons. P197 predominated at proximal axonal levels; P200 displayed a relatively uniform distribution; and P205 and P210 became increasingly prominent at more distal axonal levels, paralleling the distribution of the stationary neurofilament network.(ABSTRACT TRUNCATED AT 400 WORDS)

The early development of retinal ganglion cells with uncrossed axons in the mouse: retinal position and axonal course

Development ◽  
1990 ◽  
Vol 108 (3) ◽  
pp. 515-523 ◽  
Author(s):  
R.J. Colello ◽  
R.W. Guillery
Keyword(s):  
Developmental Stages ◽  
Ganglion Cells ◽  
Optic Chiasm ◽  
Temporal Part ◽  
Retinal Ganglion ◽  
Retinal Position ◽  
Optic Stalk ◽  
Carbocyanine Dye ◽  
Optic Axons ◽  
Dorsal Retina

The carbocyanine dye, DiI, has been used to study the retinal origin of the uncrossed retinofugal component of the mouse and to show the course taken by these fibres through the optic nerve and chiasm during development. Optic axons first arrive at the chiasm at embryonic day 13 (E13) but do not cross the midline until E14. After this stage, fibres taking an uncrossed course can be selectively labelled by unilateral tract implants of DiI. The earliest ipsilaterally projecting ganglion cells are located in the dorsal central retina. The first sign of the adult pattern of distribution of ganglion cells with uncrossed axons located mainly in the ventrotemporal retina is seen on embryonic day 16.5, thus showing that the adult line of decussation forms early in development. A small number of labelled cells continue to be found in nasal and dorsal retina at all later stages. At early stages (E14-15), retrogradely labelled uncrossed fibres are found in virtually all fascicles of the developing nerve, intermingling with crossed axons throughout the length of the nerve. At later stages of development (E16-17), although uncrossed fibres pass predominantly within the temporal part of the stalk, they remain intermingled with crossed axons. A significant number of uncrossed axons also lie within the nasal part of the optic stalk. The position of uncrossed fibres throughout the nerve in the later developmental stages is comparable to that seen in the adult rodent (Baker and Jeffery, 1989). The distribution of uncrossed axons thus indicates that positional cues are not sufficient to account for the choice made by axons when they reach the optic chiasm.

Dendritic competition in the developing retina: Ganglion cell density gradients and laterally displaced dendrites

1993 ◽  
Vol 10 (2) ◽  
pp. 313-324 ◽  
Author(s):  
Rafael Linden
Keyword(s):  
Density Gradient ◽  
Cell Density ◽  
Time Course ◽  
Ganglion Cells ◽  
Lateral Displacement ◽  
Optic Tract ◽  
Density Gradients ◽  
Temporal Asymmetry ◽  
Dendritic Arbors ◽  
Contralateral Eye

AbstractDendrites of retinal ganglion cells (RGCs) tend to be distributed preferentially toward areas of reduced RGC density. This, however, does not occur in the retina of normal pigmented rats, in which it has been suggested that the centro-peripheral gradient of RGC density is too shallow to provide directional guidance to growing dendrites. In this study, laterally displaced dendrites of RGCs retrogradely labeled with horseradish peroxidase were related to cell density gradients induced experimentally in the rat retina. Neonatal unilateral lesions of the optic tract produced retrograde degeneration of contralaterally projecting RGCs, but spared ipsilaterally projecting neurons in the same retina. These lesions created an anomalous temporal to nasal gradient of cell density across the decussation line, opposite to the nasal to temporal gradient found along the same axis in either normal rats or rats that had the contralateral eye removed at birth. RGCs in rats that received optic tract lesions had their dendrites displaced laterally toward the depleted nasal retina, while in either normal or enucleated rats there was no naso-temporal asymmetry. The lateral displacement affected both primary dendrites and higher-order branches. However, the gradient of cell density after optic tract lesions was less steep than the gradient in either normal or enucleated rats. To test for the presence of steeper gradients at early stages of development, RGC density gradients were also examined at postnatal day 5 (P5). In normal rats, the RGCs were homogeneously distributed throughout the retina, while rats given optic tract lesions at birth already showed a temporo-nasal density gradient at P5. Still, this anomalous gradient was less steep than that found in normal adults. It is concluded that the time course, rather than the steepness of the RGC density gradient, is the major determinant of the lateral displacement of dendritic arbors with respect to the soma in developing RGCs. The data are consistent with the idea that the overall shape of dendritic arbors depends in part on dendritic competition during retinal development.

Fibre order in the normal Xenopus optic tract, near the chiasma

Development ◽  
1984 ◽  
Vol 83 (1) ◽  
pp. 1-14
Author(s):  
J. W. Fawcett ◽  
J. S. H. Taylor ◽  
R. M. Gaze ◽  
P. Grant ◽  
E. Hirst
Keyword(s):  
Optic Nerve ◽  
Small Groups ◽  
Optic Nerve Head ◽  
Tritiated Thymidine ◽  
Optic Tract ◽  
Peripheral Retina ◽  
Retinal Lesions ◽  
Dorsal Retina

In juvenile Xenopus retinotopic fibre order in the optic tract near the chiasma was investigated by labelling small groups of optic fibres from peripheral retina with HRP. This selective fibre labelling with HRP was combined with autoradiography following administration of tritiated thymidine to the eye, so that the HRP-labelled fibres could be located within the borders of the optic tract. Fibres arising from the periphery of all four retinal quadrants were superficially located in the optic tract near the chiasma, with dorsal retinal fibres showing the greatest tendency to travel deep in the diencephalon. Retinal lesions closer to the optic nerve head labelled fibres which ran deeper in the optic tract. Near the chiasma, fibres from ventral retina tended to group rostrally while fibres from dorsal retina tended to group caudally. However, no obvious localization of fibres arising in temporal or nasal retina was seen in the lower optic tract.

A developmental and ultrastructural study of the optic chiasma in Xenopus

Development ◽  
1988 ◽  
Vol 102 (3) ◽  
pp. 537-553
Author(s):  
M.A. Wilson ◽  
J.S. Taylor ◽  
R.M. Gaze
Keyword(s):  
Optic Nerve ◽  
Cell Mass ◽  
Light And Electron Microscopy ◽  
Optic Tract ◽  
Retinal Ganglion ◽  
Intercellular Spaces ◽  
Optic Chiasma ◽  
Cell Processes ◽  
Optic Axons ◽  
The Brain

The structure of the optic chiasma in Xenopus tadpoles has been investigated by light and electron microscopy. Where the optic nerve approaches the chiasma, a tongue of cells protrudes from the periventricular cell mass into the dorsal part of the nerve. Glial processes from this tongue of cells ensheath fascicles of optic axons as they enter the brain. Coincident with this partitioning, the annular arrangement of axons in the optic nerve changes to the laminar organization of the optic tract. Beyond the site of this rearrangement, all newly growing axons accumulate in the ventral-most part of the nerve and pass into the region between the periventricular cells and pia which we have called the ‘bridge’. This region is characterized by a loose meshwork of glial cell processes, intercellular spaces and the presence of both optic and nonoptic axons. In the bridge, putative growth cones of retinal ganglion cell axons are found in the intercellular spaces in contact with both the glia and with other axons. The newly growing axons from each eye cross in the bridge at the midline and pass into the superficial layers of the contralateral optic tracts. As the system continues to grow, previous generations of axon, which initially crossed in the existing bridge, are displaced dorsally and caudally, forming the deeper layers of the chiasma. At their point of crossing in the deeper layers, these fascicles of axons from each eye interweave in an intimate fashion. There is no glial segregation of the older axons as they interweave within the chiasma.

Pathways of regenerated retinotectal axons in goldfish

Development ◽  
1986 ◽  
Vol 93 (1) ◽  
pp. 1-28
Author(s):  
Claudia A. O. Stuermer
Keyword(s):  
Optic Nerve ◽  
Retinal Ganglion Cells ◽  
Normal Development ◽  
Ganglion Cells ◽  
Optic Tract ◽  
Spatiotemporal Pattern ◽  
Retinal Ganglion ◽  
Retinal Axons ◽  
Age Related ◽  
Regenerated Fibres

This study investigates the order of regenerating retinal axons in the goldfish. The spatiotemporal pattern of axon regrowth was assessed by applying horseradish peroxidase (HRP) to regenerating axons in the optic tract at various times after optic nerve section and by analysing the distribution of retrogradely labelled ganglion cells in retina. At all regeneration stages labelled ganglion cells were widely distributed over the retina. There was no hint that axons from central (older) ganglion cells might regrow earlier, and peripheral (younger) ganglion cells later, as occurs in normal development. The absence of an age-related ordering in the regenerated optic nerve was demonstrated by labelling a few axon bundles intraorbitally with HRP (Easter, Rusoff & Kish, 1981) caudal to the previous cut. The retrogradely labelled cells in retina were randomly distributed in regenerates andnot clustered in annuli as in normals. Tracing regenerating axons which were stained anterogradelyfrom intraretinal HRP applications or retrogradely from single labelled tectal fascicles illustrated the fact that the regenerating axons coursed in abnormal routes in the optic nerve and tract. On the surface of the tectum regenerated fibres re-established a fascicle fan. The retinal origin of tectal fascicles was assessed by labelling individual peripheral, intermediate and rostral fascicles with HRP. The retrogradely labelled ganglion cells in the retina were often more widely distributed than in normals, but were mostly found in peripheral, intermediate and central retina, respectively. The order of fibre departure from each tectal fascicle was revealed by placing HRP either on the fascicle's proximal or on its distal half. With proximal labelling sites labelled ganglion cells were found in the temporal and nasal retina, and with distal labelling sites labelled ganglion cells were confined to nasal retina only. Further, the axonal trajectories of anterogradely labelled dorsotemporal retinal ganglion cells were compared to those of dorsonasal retinal ganglion cells in tectal whole mounts. Dorsotemporal axons were confined to the rostral tectal half, whereas dorsonasal axons followed fascicular routes into the fascicles' distal end and reached into caudal tectum. This suggests that the fibres exited along their fascicle's course in a temporonasal sequence. Thus in the tectum, fibres in fascicles restore a gross spatial and age-related order and tend to follow their normal temporonasal sequence of exit.

Abnormally high variability in the uncrossed retinofugal pathway of mice with albino mosaicism

Development ◽  
1987 ◽  
Vol 101 (4) ◽  
pp. 857-867 ◽  
Author(s):  
R.W. Guillery ◽  
G. Jeffery ◽  
B.M. Cattanach
Keyword(s):  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Gene Dosage ◽  
Optic Tract ◽  
High Variability ◽  
Retinal Ganglion ◽  
Rare Occurrence ◽  
Autosome Translocation ◽  
Open Question ◽  
The Relationship

Female mice showing albino mosaicism due to an X-autosome translocation [Is(In7;X)Ct] have been studied in order to investigate the relationship between the distribution of melanin and the formation, early in development, of the abnormally small uncrossed retinofugal pathway characteristically found in all albino mammals. Earlier evidence indicates that cells normally bearing melanin play a role in producing the abnormality. In the mosaic mice, the albino gene is expressed in only about half of the cells due to random X-inactivation and the patches of normal and albino cells are extremely small relative to total retinal size (less than 1/50). We argued that if all the cells that would normally bear melanin play a role in producing the albino abnormality then the mosaic mice would have a pathway abnormality, about half the size of that in the albino mice. If, however, only a small patch of these cells plays a role, as has been proposed in earlier studies, then one would expect the size of the uncrossed pathway to be highly variable in the mosaic mice. The size of the uncrossed pathway was assessed by placing horseradish peroxidase in the region of the optic tract and lateral geniculate nucleus unilaterally and then counting the number of retrogradely labelled retinal ganglion cells on the same side. The mosaic mice showed a highly variable uncrossed pathway. In some of the mosaic mice, it was the same size as in the albinos and, in others, it was the same size as in normally pigmented mice. Surprisingly, in a small number of mosaic mice, the uncrossed pathway was larger than normal. Whether this relatively rare occurrence of a supernormal uncrossed pathway is due to the higher gene dosage or to the translocation itself remains an open question.

Distribution of uncrossed and crossed retinofugal axons in the cat optic nerve and their relationship to patterns of fasciculation

1990 ◽  
Vol 5 (1) ◽  
pp. 99-104 ◽  
Author(s):  
Glen Jeffery
Keyword(s):  
Optic Nerve ◽  
Optic Tract ◽  
Relative Increase ◽  
Lateral Aspect ◽  
Optic Nerves ◽  
Caudal Region ◽  
Lateral Extent ◽  
Optic Axons ◽  
Horseradish Peroxide ◽  
Caudal Segment

AbstractThe course of optic axons that take different routes at the chiasm have been traced through horizontally sectioned optic nerves in the cat, after unilateral injections of horseradish peroxide into the optic tract. Behind the eye and for most of the course of the nerve, nearly all of the axons that remain uncrossed at the chiasm are located in a retinotopically appropriate position, in the lateral aspect of the nerve. However, in the most caudal segment of the nerve an increasing proportion of these axons are located in regions that are retinotopically inappropriate. Just before the nerve joins the chiasm, uncrossed axons can be found across the full medio-lateral extent of the nerve, although there is still a relative increase in their density laterally.Labeled axons that cross at the chiasm course in a relatively parallel manner along the greater proportion of the nerve. However, in the caudal segment of the nerve their relative positions change and they appear to course in an irregular manner. This occurs where the uncrossed projection becomes increasingly more widespread.Axons in the optic nerve are grouped into fascicules. This pattern of organization also changes in the caudal region of the nerve. Although clear fascicular patterns are present along the greater part of the nerve, they become progressively less distinct caudally. The change in the pattern of fasciculation occurs over the same region of the nerve as the relative changes in axon trajectory and distribution.These results demonstrate that irrespective of chiasmatic route, optic axons in the cat are reorganized in the caudal segment of the nerve. This reorganization is not confined to changes in relative axon position, but is reflected in the structure of the nerve by the change of axon grouping from a fascicular to a non-fascicular arrangement.

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