Long term regeneration of contralateral and induced ipsilateral retinal projections to the remaining optic tectum ofRutilus rutilus

The regeneration of optic tract fibers hs been investigated in Rutilus kept at 18-20 degrees C, 6-7 months after ablation of one optic tectum and simultaneous section of the optic nerve from the contralateral eye. The labeling of the optic fibers obtained following injection of either tritiated proline or HRP in either of the eyes showed the existence of a normal contralateral retino-tectal projection to strata opticum, fibrosum et griseum superficial (SFGS), griseum centrale, and album centrale. Furthermore, it demonstrated the presence of a conspicuous newly-formed ipsilateral retino-tectal projection to both superficial and deep layers of SFGS in the form of horizontal bands. The partial overlapping of ipsi- and contralateral projections in SFGS was confirmed by a double-labeling technique (HRP and tritiated proline). The results suggest a retinal hyperinnervation of the remaining optic tectum.     

A critical period in the development of tectal neurons in the chick, as revealed by early enucleation

To further study the existence of a critical trophic period in the development of the chick optic tectum¹⁷, during which the presence of retinal synapses is essential to the continued growth of tectal neurons, we have unilaterally enucleated embryos between stages 14–20 and allowed survival until stages 35–43. If the critical trophic period is between stages 40–44, as previously reported¹⁷, then we reasoned that early removal of the eye might not have any effect on tectal development until the critical period. We assessed tectal neuron survival by staining for degeneration in the efferent projections of tectal neurons. In early enucleates, degeneration was present from stages 37–43, and the severity of the degeneration was much reduced in comparison to animals enucleated during the critical period.These findings substantiate the proposition that there is a critical period late in chick tectal development. However, because the degeneration in tectal projections is less intense than in animals enucleated during the critical period, we suggest that the early enucleation has permitted axons from the remaining eye to be routed to the deafferented tectum, where they may help to sustain a portion of the tectal neurons through the critical period. Moreover, the somewhat earlier appearance of degeneration in tectal efferent pathways of early enucleates suggests that a subtle trophic relationship between retina and tectum may exist prior to stage 40, even though this relationship is not revealed when enucleations are performed later, as between stages 35–40 (ref. 17).     

On the formation of eye dominance stripes and patches in the doubly-innervated optic tectum of the chick

By surgically dividing the region of the presumptive optic chiasm in chick embryos on the third day of incubation (around stage 15), we have been able to induce substantial numbers of optic nerve fibers to grow aberrantly into the ipsilateral optic tract. As a result, many of the visual centers that are normally innervated only by fibers from the contralateral retina received fibers from both eyes. The proportion of fibers going to each tectal lobe varied from case to case, but in about one-third of the animals the tectal lobes received approximately equal numbers of fibers from each eye. In animals that survived until embryonic days 17-19 (which is beyond the period of retinal ganglion cell death) labeling of the two eyes with WGA-HRP and [3H]proline respectively, revealed a pattern of sharply defined eye dominance stripes or patches in the stratum griseum et fibrosum superficiale (SGFS) of the optic tectum, and in the ventral lateral geniculate nucleus. Less clearly segregated eye dominance zones were seen in the ectomammillary nucleus and the nucleus externus. The size and distribution of the stripes varied depending on the number of fibers projecting from each eye to a given tectal lobe; the minimum size was about 75 micron, while the maximum was large enough to occupy almost the entire tectal lobe. In animals in which the tectal input from the two eyes was roughly equal, the stripes varied in width between 75 micron and about one-third of the surface of the tectal lobe. The orientation of the stripes was consistently orthogonal to the direction of fiber ingrowth from the optic tract. From the earliest stages of optic fiber ingrowth, the fibers from the two eyes are completely intermixed in the stratum opticum (SO). However, on embryonic day 12, shortly after they have begun to penetrate into the SGFS, they are already segregated into stripes, although the stripe borders are very fuzzy. This suggests that the fibers from the two eyes may overlap at this stage. The phase of stripe formation coincides with that of naturally occurring retinal ganglion cell death, and we suggest that the two processes are interlinked.     

Organization of the visual system in larval lampreys: an HRP study.

The organization of the visual system of larval lampreys was studied by anterograde and retrograde transport of HRP injected into the eye. The retinofugal system has two different patterns of organization during the larval period. In small larvae (less than 60-70 mm in length) only a single contralateral tract, the axial optic tract, is differentiated. This tract projects to regions in the diencephalon, pretectum, and mesencephalic tegmentum. In larvae longer than 70-80 mm, there is an additional contralateral tract, the lateral optic tract, which extends to the whole tectal surface. In addition, ipsilateral retinal fibers are found in both small and large larvae. Initially, the ipsilateral projection is restricted to the thalamus-pretectum, but it reaches the optic tectum in late larvae. Changes in the organization of the optic tracts coincide with the formation of the late-developing retina and consequently, the origin of the optic tracts can be related to specific retinal regions. The retinopetal system is well developed in all larvae. Most retinopetal neurons are labeled contralaterally and are located in the M2-M5 nucleus of the mesencephalic tegmentum, in the caudolateral mesencephalic reticular area and adjacent ventrolateral portions of the optic tectum. Dendrites of these cells are apparent, especially those directed dorsally, which in large larvae extend to the optic tectum overlapping with the retino-tectal projection. These results indicate that in lampreys, visual projections organize mainly during the blind larval period before the metamorphosis, their development being largely independent of visual function.     

The anatomical organization of retinal projections in the shark Scyliorhinus canicula with special reference to the evolution of the selachian primary visual system

The retinal projections of the shark Scyliorhinus canicula were investigated using both the degeneration technique after eye removal and the radioautographic method following the intraocular injection of various tritiated tracers (proline, leucine, fucose, adenosine). The results showed contralateral projection via different optic tract components (TOM, AOT, TOm, TOl, ROVm, RODm) to various areas and nuclei of the hypothalamus (NSC), thalamus (NODLAT, NODMAT, NTTOM, NOVT, NODPT), pretectum (NOPC, NOCPd, NOCPv), tectum (SFGS, SGI) and mesencephalic tegmentum (AOTMd, NOTMv). Ipsilateral retinal projections were found to arborize within 7 distinct zones at the hypothalamic (NSC), thalamo-pretectal (NODLAT, NTTOM, NOVT, NOPC, NOCpd) and tectal (SFGS) levels. A comparison of the data with those previously obtained in different species of elasmobranchs and batoids indicate the existence of a common and consistent pattern of organization of the primary visual system in all selachians. Many of the discrepancies reported in studies on the organization of selachian retinal projection may be listed to methodological differences and/or interspecies variations in the cytoarchitecture of the different visual centers. Moreover, a comparison of the primary visual system of more primitive squalomorph sharks with that of the more advanced galeomorph sharks and batoids suggests that this system evolved through an increase in the neuronal density of the target structures and transformations in the dendritic configurations of the postsynaptic neurons rather than through an increase in the total number of projection zones.     

Neuronal death during development in the isthmo-optic nucleus of the chick: sustaining role of afferents from the tectum

Neurons have been counted in the isthmo-optic nucleus following lesions of the optic tectum, its main source of afferents. Late lesions, made at 10.8-12.2 days of incubation, were employed as they cause the fewest non-specific side effects. The lesions spared the isthmo-optic tract, and although they caused many retinal ganglion cells to die, the degeneration did not spread to the inner nuclear layer, which contains the target cells of the isthmo-optic fibers. Hence the effects on the isthmo-optic nucleus were due to its being deprived of afferents. Even in unoperated embryos, 60% of the isthmo-optic neurons are known to die between embryonic days 12 and 17. The tectal lesions greatly increased the cell loss ipsilaterally; this was due to cell death, since other explanations such as migration away or differential cellular shrinkage have been ruled out. The fact that additional neuronal death occurred mainly during the latter half of the period of natural cell death implies that the tectal afferents are important for the survival of the isthmo-optic neurons during this latter half, but not before.     

The anatomical organization of retinal projections in the shark Scyliorhinus canicula with special reference to the evolution of the selachian primary visual system

The retinal projections of the shark Scyliorhinus canicula were investigated using both the degeneration technique after eye removal and the radioautographic method following the intraocular injection of various tritiated tracers (proline, leucine, fucose, adenosine). The results showed contralateral projection via different optic tract components (TOM, AOT, TOm, TOI, ROVm, RODm) to various areas and nuclei of the hypothalamus (NSC), thalamus (NODLAT, NODMAT, NTTOM, NOVT, NODPT), pretectum (NOPC, NOCPd, NOCPv), tectum (SFGS, SGI) and mesencephalic tegmentum (AOTMd, NOTMv). Ipsilateral retinal projections were found to arborize within 7 distinct zones at the hypothalamic (NSC), thalamo-pretectal (NODLAT, NTTOM, NOVT. NOPC, NOCpd) and tectal (SFGS) levels.A comparison of the data with those previously obtained in different species of elasmobranchs and batoids indicate the existence of a common and consistent pattern of organization of the primary visual system in all selachians. Many of the discrepancies reported in studies on the organization of selachian retinal projection may be listed to methodological differences and/or interspecies variations in the cytoarchitecture of the different visual centers. Moreover, a comparison of the primary visual system of more primitive squalomorph sharks with that of the more advanced galeomorph sharks and batoids suggests that this system evolved through an increase in the neuronal density of the target structures and transformations in the dendritic configurations of the post-synaptic neurons rather than through an increase in the total number of projection zones.     

Control of neuronal survival by anomalous targets in the developing brain

Described here is an aberrant parabigeminothalamic projection that follows neonatal lesions of the superior colliculus in rats, with evidence that this anomalous projection may sustain a normal number of neurons in the parabigeminal nucleus after early removal of the latter's tectal target. The aberrant projection was traced radioautographically to the tectorecipient zone of the lateral posterior nucleus after an injection of tritiated amino acid in the parabigeminal nucleus. Histochemical staining for cholinesterase revealed an anomalous patch of high enzyme activity in register with both the aberrant parabigeminothalamic projection and an abnormal retinal projection that also follows tectal lesions. Histochemical staining after either binocular enucleation or a tegmental lesion made simultaneous with the tectal ablation showed that the anomalous enzyme patch is a reliable marker of the aberrant parabigeminothalamic projection. It was also shown that the retinal projection is not needed for the formation of the anomalous parabigeminothalamic pathway. Ablation of the superior colliculus at birth failed to produce a net cell loss in the contralateral middle division of the parabigeminal nucleus after the period of natural neuronal death. Lesions extending toward the anomalous terminal field in the lateral posterior nucleus, however, prevented the survival of a normal number of neurons in the parabigeminal nucleus. When the unilateral tectal ablation was made together with a lesion of the ipsilateral posterior neocortex that produced cell loss in the thalamus, the number of neurons remaining in the middle division of the contralateral parabigeminal were linearly related to the cell content of the lateral posterior nucleus. We conclude that the anomalous target in the tectorecipient zone of the lateral posterior nucleus effectively replaces the normal projection field in the superior colliculus, with regard to the trophic requirements for neuronal survival during development of the parabigeminal nucleus.     

Ultrastructural evidence of the formation of synapses by retinal ganglion cell axons in two nonstandard targets

After unilateral ablation of the optic tectum in the frog (Rana pipiens), retinal ganglion cell axons enter the lateral thalamic neuropil in large numbers. This area is normally a target of the tectal efferent projection but is not innervated directly from the retina in normal frogs nor in frogs undergoing optic nerve regeneration in the presence of an intact tectum. The ability of retinal axons to form synaptic contacts in this nonstandard target, previously suspected only from light microscope studies, has been ultrastructurally verified in the present investigation. Retinal axon terminals were selectively labeled for light and electon microscope study by introducing horseradish peroxidase (HRP) into the optic nerve 73-413 days after unilateral ablation of the contralateral optic tectum. In some of the frogs, the optic nerve had also been crushed to test the ability of retinal axons regenerating over a long distance to form this connection. The HRP-labeled retinal axon terminals had the same untrastructural morphology whether located in the lateral thalamic neuropil or in the correct regions of projection, e.g., the lateral geniculate complex. They contained clear, spherical synaptic vesicles and made Gray type I synapses on the unlabeled postsynaptic dendrites. The magnitude of the projection was disproportionately greater in animals having complete or nearly complete tectal ablation than in a specimen in which the lesion was significantly incomplete. An aberrant projection was also observed in the nucleus isthmi in some of the specimens. These findings have significance for chemoaffinity theories of the specification of synaptic connections in that the ability of retinal axons to synapse in nonstandard targets in this experimental context may be considered evidence for the expression of appropriate cell-surface recognition-molecules by the abnormally targeted postsynaptic neurons. The likelihood that the expression of these postsynaptic labels is normally repressed transynaptically by molecular signals from the intact tectal input is discussed.     

Mapping the normal and regenerating retinotectal projection of goldfish with autoradiographic methods

In normal goldfish, lesions of various size were made in nasal or temporal retina immediately prior to retinal labeling with tritiated proline. The resulting gaps in retinal innervation of tectum indicated that the projection is retinotopographically ordered to a precision of about 50 μm. Similarly, acute tectal incisions transecting the optic pathways were combined with immediate retinal labeling. The resulting tectal denervation confirmed that most fibers follow highly ordered paths through the stratum opticum of tectum; but a few fibers were found to follow unusual paths to their appropriate tectal positions. In other fish, the optic nerve was crushed. At various times afterwards, retinotopography and pathway order were similarly analyzed by making retinal lesions or tectal incisions just prior to labeling. For up to 40 days after crush, the projection lacked any refined retinotopic order. Only a gross topography could be demonstrated. Over several months, retinotopography gradually improved eventually approaching that of normals. Correlated with this was an initial stereotypic growth through the pathways of the stratum opticum followed by a long period of highly anomalous growth through the innervation layer. Evidently, many regenerated fibers grew in through inappropriate routes to the wrong region of tectum but subsequently arrived at their appropriate locus by circuitous routes within the innervation layer.     

Retinotopic organization in the development of the young trout Salmo gairdneri Rich

The progression of the retinotopic organization in the optic nerve projections to the contralateral thalamus and tectum was studied in Salmo gairdneri from hatching stage to 3 month old stage. After quadratic lesions of the temporal, dorsal, nasal, or ventral retina, the animals were separated in two groups: one used for Fink and Heimer method or electron microscopic observation and the other one for radioautography after injection in the operated eye of 14C or 3H proline. The analysis of the projections of each retinal quadrant shows that: Projections to thalamus and pretectum are ignorganized and appear progressively during development. On the contrary in tectum and corpus geniculatum, the visual projections are retinotopically organized since hatching. In the whole retino-tectal system, two subsystems develop differently: the naso-ventral retina reaches precociously its permanent target (the posterior tectum), the temporo-dorsal part of the retina links to the anterior tectum and shifts laterally during the first month after hatching, from medial to antero-lateral tectum for temporal projections. The shifting of projections is correlated with development of the medial fascicle of the optic tract. So it appears that the pathways play an important role in the spatio-temporal ordered pattern of terminations of retinal fibers on the tectal surface during development.     

Retinotopic organization of the developing retinotectal projection in the zebrafish embryo

Developing retinal axons in the zebrafish embryo were stained with HRP or with the fluorescent dyes dil and diO to study the formation of the retinotectal projection. Retinal axons leave the eye at 34-36 hr postfertilization (PF), invade the tectum at 46-48 hr PF, and innervate the tectal neuropil at 70-72 hr PF. Dorsal and ventral axons occupy separate aspects of the optic nerve and tract and pass into their retinotopically appropriate ventral and dorsal hemitectum, respectively. Nasal and temporal axons are segregated in the nerve, mixed in the tract, and are coextensive over the rostral half of tectum until 56 hr PF. They then segregate again, due to the progression of nasal axons into the open caudal tectum. Thus, at 70-72 hr PF, dorsal and ventral as well as temporal and nasal axons occupy their retinotopically appropriate tectal quadrants. After ablation of the temporal retina prior to the time of axonal outgrowth, the nasal axons bypass the vacant rostral tectum to terminate in the caudal tectal half. Temporal axons in the absence of nasal axons remain restricted to their appropriate rostral tectal half, suggesting that nasal and temporal axons possess a preference for their retinotopically appropriate tectal domains. Measurements of individual terminal arbors and the tectal areas in embryos and in adult zebrafish showed that individual arbors are large with respect to the embryonic tectum but are about 14-15 times smaller than in the adult. However, the proportion of tectum covered by embryonic arbors is about 7 times larger than in the adult, suggesting that a higher precision of the adult projection is achieved as a result of a greater enlargement of the tectum than of the arbors.     

The lens has a specific influence on optic nerve and tectum development in the blind cavefish Astyanax

We used the teleost Astyanaxmexicanus to examine the role of the lens in optic nerve and tectum development. This speciesis unusually suited for studies of nervous system development and evolution because of its two extant forms: an eyed surface dwelling (surface fish) and several blind cave dwelling (cavefish) forms. Cavefish embryos initially form eye primordia, but the lens eventually dies by apoptosis, then the retina ceases to grow, and finally the degenerating eyes sink into the orbits. Transplantation of an embryonic surface fish lens into a cavefish optic cup restores eye development. We show here that retinal nerve fibers are formed and project to the optic tectum in cavefish embryos. In adult cavefish that have completed lens degeneration, however, the number of retinal axons in the optic nerve is substantially reduced compared to surface fish. The presumptive brain domains of embryonic cavefish are not altered relative to surface fish based on expression of the regional marker genes Pax6, Pax2.1, and engrailed2. In contrast, the adult cavefish brain is elongated, the optic tectum is diminished in volume, and the number of tectal neurons is reduced relative to surface fish. Unilateral transplantation of an embryonic surface fish lens into a cavefish optic cup increases the size of the optic nerve, the number of retinotectal projections from the restored eye, and the volume and neuronal content of the contralateral optic tectum. The results suggest that the lens has a specific influence on optic nerve and tectum development during eye growth in Astyanax.     

The optic system of the teleost Cichlasoma biocellatum

The retinal projections of the fresh water teleost. Cichlasoma biocellatum, were examined using a modification of the Nauta-Gygax method following unilateral enucleations and removal of retinal quadrants. After the unilateral enucleations, degeneration was found in the fasciculus medialis nervioptici, fasciculus geniculatus tractus optici, fasciculus dorsomedialis tractus optici, and the accessory optic tract. The pretectal nucleus, nucleus corticalis, and accessory optic nucleus contained debris of terminal degeneration. The majority of the optic fibers terminated in five layers in the optic tectum. The quadrant removals showed that fibers from the retinal quadrants formed layers in the ribbon shaped optic nerve running the width of the nerve. The dorsal to ventral arrangement of the fibers was: dorsal nasal quadrant; dorsal temporal quadrant; ventral nasal quadrant; and the ventral temporal quadrant. The fibers from only the posterior half of the retina supplied the fasciculus geniculatus tractus optici and the corpus geniculatum laterale. Fibers from the anterior half of the retina supplied the accessory optic tract and nucleus. All other tracts and nuclei examined received fibers from all the retinal quadrants. The projection of the retinal quadrants to the tectal quadrants was specific and always formed five layers of degeneration.     

An autoradiographic study of the retinofugal projections in the shark, Hemiscyllium plagiosum

The retinofugal projections in the shark, Hemiscyllium plagiosum were studied after unilateral eye injection of tritiated proline. The results showed that each eye in this animal projects not only to the contralateral side of the brain but also to several ipsilateral visual centers including the nucleus suprachiasmaticus, ventrolateral nucleus of the optic tract and the optic tectum. These results suggest that some of the visual centers in this animal receive direct retinal inputs from both eyes as is the case in many other animals and most notably in mammals.     

Experimental anatomic study of the topography of the retinofugal projections in Discoglossus pictus (Amphibia, Anura). II. The tectum: existence of a double-system of primary optic projections

The possibility of retinotopic organization of bilateral retinotectal projection was studied by fotal retinal lesions followed by the Fink-Heimer technique. This work in Discoglossus pictus (Amphibia, Anura) shows two types of direct visual projections: a contralateral projection within the tectal layer 9 and a bilateral projection on tectal layer F of Potter (1969). The ipsilateral projection within tectal layer 9, earlier described after enucleation (Picouet et Clairambault, 1977), is not observed here. We discuss about reasons we failed to reveal it. Although appearing to be grossly in accord with data of literature, the retinotopic pattern of "classical" retinotectal projection (on layer 9) of Discoglossus presents some differences as the overlap of quadratic retinal projections. The anatomical tectal retinotopy appears less precise that physiologic retinotopy. The bilateral projections on layer F are characterised by medial (and specially medioposterior) location and the complete absence of retinotopy. All lesions in different parts of retina lead degeneration which take place in a series of distinct loci in the dorsal layer F. We discuss about a possible participation of axial optic tract to this projection.     

Retinal fibers alter tectal positional markers during the expansion of the retinal projection in goldfish

Although widely accepted, the theory, that neurones carry immutable cytochemical markers which specify their synaptic connections, is not consistent with plastic reorganizations. Half retinal fish were therefore tested for changed markers following expansion. Optic nerve crush at the time of the half retinal ablation resulted in regeneration of a normal, restricted projection; but nerve crush following expansion (many months later) resulted in reestablishment of the expanded projection, assessed both by electrophysiological mapping and by radioautography. Since this implied changed markers, the half retina and tectum were tested independently using the ipsilateral tectum and eye as controls. In normal fish, removal of one tectum and deflection of the corresponding optic tract toward the remaining tectum resulted in regeneration of a positionally normal but ipsilateral map. In experimental fish, after the half retina had expanded its projection to the contralateral tectum, its optic tract was deflected to the control tectum. After 40 days it had regenerated a normal, restricted map indicating that the retinal markers had not changed. Such restricted projections did not expand in the presence of the normal projection even after a year or more. Similarly, the optic tract from the normal eye was deflected to cause innervation of the tectum containing the expanded half retinal projection. After 40 days, the projection regenerated from the normal eye was similar to the expanded half retinal projection. Areas of the normal retina corresponding to the missing areas of the half retina were not represented. Tectal markers had been altered by the half retinal fibers. In a final group, tecta were denervated and tested at various intervals by innervation from ipsilateral half retinal eyes. After five months of denervation, the regenerating fibers were no longer restricted to the rostral tectum but formed an expanded projection initially. Apparently tectal markers are induced by the retinal fibers, changed during expansion, and disappear during long-term denervation.     

The development and restriction of the ipsilateral retinofugal projection in the chick

Although it is generally believed that the central projections of the retina in birds are entirely crossed, using wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) as an anterograde tracer, we have found that in normal posthatched chicks there is a small ipsilateral retinofugal projection to the diencephalon and midbrain. Most of the ipsilateral fibers appear to be directed to the lateral anterior and dorsolateral anterior nuclei of the thalamus, to the pretectal region, and to the ectomammillary nucleus and the adjoining nucleus externus. Even in the best preparations the numbers of ipsilateral fibers are so small that it is hardly surprising that they have been overlooked in previous axonal degeneration and autoradiographic experiments. A significantly larger ipsilateral retinal projection develops during the second week of incubation. The ipsilaterally directed fibers can be first seen on the fifth day of incubation and their numbers appear to increase until about embryonic day 12. At this stage the projection involves substantially more fibers than at hatching and is also more extensive in its distribution; in fact, in its general organization (but not its size) it closely parallels the normal crossed retinofugal system, contributing fibers to essentially all the primary visual relay nuclei in the diencephalon and midbrain and to much of the optic tectum, where the densest projection is to its caudomedial aspect. During the second week of incubation there is also a small number of retinal fibers, which after crossing in the optic chiasm, recross the midline in the posterior and tectal commissures (and also in the tectal roof plate), before ending in the pretectal region of the ipsilateral side. In addition, there is a markedly aberrant projection from the retina into the contralateral optic nerve. Most of the ipsilateral retinal fibers are eliminated between the twelfth and sixteenth days of incubation, and by day 17 the ipsilateral projection is reduced to its mature form. The progressive reduction in the ipsilateral projection occurs at a time when it is known (from other studies) that there is an appreciable loss of retinal ganglion cells; but whether the reduction is due to neuronal death or to the selective elimination of ipsilateral axon collaterals remains to be determined. The existence of a significant ipsilateral retinofugal component early in development, probably accounts, in part, for the distinctive and persistent ipsilateral projection that occurs if one eye is removed during the first few days of incubation.     

Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order

The retinotectal projection is organized in a precise retinotopic manner. We find, though, that during development the growth and arborization of temporal retinal axons within the optic tectum of chick embryos is initially imprecise. Axonal targeting errors occur along the rostral-caudal and medial-lateral tectal axes, and arbors are formed at topographically inappropriate positions. Subsequent course corrections along both tectal axes and large-scale axonal remodeling lead to the retinotopic ordering of terminal arborizations characteristic of the mature projection. The trajectories and branching patterns of temporal retinal axons labeled with Dil or DiO were determined in whole mounts of retina and tectum from chicks ranging in age from embryonic day 9 to posthatching. Within the retina, labeled retinofugal axons travel in a compact bundle but do not maintain strict neighbor relations, as they course to the optic fissure. The axons enter the contralateral tectum at its rostral edge and grow caudally. Many extend well past their appropriate terminal zone within rostral tectum; a proportion of these later reverse their direction of growth. Many axons grow onto the tectum at incorrect positions along the medial-lateral tectal axis. Some correct this error in a directed manner by altering their trajectory or extending collateral branches at right angles. About 80% of the positional changes of this type are made in the direction appropriate to correct axon position, and thus are likely a response to tectal positional cues. After maturation of retinotopic order, about half of the axons that project to a mature terminal zone have made abrupt course corrections along one or both tectal axes, indicating that initially mistargeted axons can establish appropriately positioned arbors and survive. The development of temporal axons within the tectum is characterized by 3 phases: elongation, branch and arbor formation, and remodeling. After considerable rostrocaudal elongation, an axon typically develops numerous side branches and arbors, many at inappropriate locations. Most arbors are formed by side branches that develop as interstitial collaterals; few axons grow directly to their appropriate terminal zone and arborize. Aberrant arbors, and axons and axon segments that fail to form arbors in the appropriate terminal zone, are rapidly eliminated over about a 2 d period. Axon degeneration appears to play a role in this remodeling process.