Retinal ganglion beta cells project transiently to the superior colliculus during development.

Ramoa, Ary S.; Campbell, G.; Shatz, Carla J.

doi:10.1073/pnas.86.6.2061

Cited by 32 publications

(24 citation statements)

References 28 publications

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“…In cats, retinal /3 cells, which project only to the thalamus in adults, extend their trunks transiently to SC at early developmental stages (Ramoa et al, 1989). Similarly, ascending auditory, somatosensory, and cerebellar afferents to the rat thalamus initially extend rostra1 to their definitive termination sites and, in some instances, elongate into the internal capsule (Asanuma et al, 1988).…”

Section: Axonal Growth Statesmentioning

confidence: 99%

Stages of growth of hamster retinofugal axons: implications for developing axonal pathways with multiple targets

Bhide

Frost

1991

J. Neurosci.

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Neurons in many regions of the CNS (e.g., cortical areas, thalamic nuclei) are heterogeneous with regard to their afferent and efferent connections. Using the hamster retinofugal system as a model, we investigated the mechanisms by which such connectional heterogeneity arises during ontogeny. Retinal ganglion cell axons were labeled with 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate (Dil) in paraformaldehyde-fixed tissue. The fluorescent label was photoconverted to a diaminobenzidine reaction product. The morphology of the axons, including their trajectories, branching patterns, and growth cones, was studied at the level of the dorsal lateral geniculate nucleus (LGd) from embryonic day 14 to adulthood. In adult hamsters, axons of retinal ganglion cells (RGCs) are spatially segregated at the level of the lateral geniculate nucleus into a superficial optic tract, situated just beneath the pia, and an internal optic tract consisting of fascicles running parallel to the pia within the geniculate. All retinofugal axons project to the midbrain, but only superficial optic tract axons emit collaterals to the LGd. During development, axons in both divisions of the optic tract emit collaterals to the LGd, but by postnatal day 15, collaterals of internal optic tract axons are virtually entirely eliminated, whereas those of superficial optic tract axons have elaborated terminal arbors. Thus, the heterogeneity among different classes of RGCs with respect to their efferent connections emerges by the selective stabilization, by each class, of a unique subset of connections from an initially widespread set shared by all classes. Thalamic collaterals of RGC axons emerge along established axon trunks, not by bifurcation of the growing tip. This occurs after the axons have grown past the thalamus and, presumably, entered their targets in the midbrain. Growth cones at the tips of elongating axon trunks are larger in size and have a more “complex” morphology compared to the growth cones on collaterals. Axons of RGCs develop in 3 morphologically distinct growth states. First, they elongate to their most distant targets in the midbrain. Then, they simultaneously emit unbranched or poorly branched collaterals to multiple targets. Finally, they elaborate terminal arbors in their definitive targets and eliminate their other collaterals. This developmental strategy may be paradigmatic for the formation of long CNS pathways with multiple targets. Furthermore, these data document, at the single-axon level, the steps in the elaboration and withdrawal of transient neuronal projections.

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Section: Axonal Growth Statesmentioning

confidence: 99%

Stages of growth of hamster retinofugal axons: implications for developing axonal pathways with multiple targets

Bhide

Frost

1991

J. Neurosci.

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“…Thus, RGCs making inappropriate projections could be unambiguously identified. Another advantage is that RGCs retrogradely labeled with microspheres have been shown to develop normally even when examined several weeks after the original injections (Ramoa et al, 1989).…”

Section: Methodsmentioning

confidence: 99%

“…To reveal axonal projections during development, rhodamine labeled latex microspheres (Lumafluor , Bardonia, NY) were injected into the SC or IC of rats aged between PO and P5. One major reason rhodamine labeled latex microspheres were used to identity projection patterns of developing RGCs is their tendency to remain restricted to the injection site, displaying little diffusion even after several weeks (Ramoa et al, 1989). Thus, RGCs making inappropriate projections could be unambiguously identified.…”

Section: Methodsmentioning

confidence: 99%

“…Several examples of transient retinal projections have been reported over the past years: projections to the contralateral retina of rats (Bunt et al, 1981;Muller and Hollander, 1988); transient projections to the SC of the cat (Ramoa et al, 1989); topographically inappropriate projections to the SC in rats and chicks O'Leary et al, 1986); projections to nonvisual nuclei, such as the inferior colliculus, in rodents (Itaya and VanHoesen, 1982;Kato, 1983;Frost, 1984;Cooper and Cowey, 1990a,b); projections to inappropriate eye-specific geniculate lamina in cat, ferret and monkey (Rakic, 1976;Linden et al, 1981;Shatz 1983); and projections from nasal retina to the ipsilateral side of the brain in rodents, cats, ferrets and monkeys (Land and Lund, 1979;Martin et al, 1983;Insausti et al, 1984;Jacobs et al, 1984;Chalupa and Lia, 1991;Cucchiaro, 1991;Wingate and Thompson, 1994). The generalized occurrence of transient retinal projections during mammalian development raises the issue of what cell types are involved.…”

Section: Type-specificity Of Transient Retinal Projectionsmentioning

confidence: 98%

“…Similarly, RGC axon arbors within the lateral geniculate nucleus have been shown to undergo considerable changes during development (Sur et al, 1984;Sretavan and Shatz, 1986). Axonal remodeling with loss of collaterals has also been found to occur in RGCs that make a transient projection to the superior colliculus (Ramoa et al, 1989;Wingate and Thompson, 1995).…”

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confidence: 96%

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Transient retinal ganglion cells in the developing rat are characterized by specific morphological properties

Ramoa¹,

Yamasaki²

1996

J. Comp. Neurol.

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To determine whether dendritic development of mammalian retinal ganglion cells (RGCs) is affected by axonal target specificity, the morphology of three populations of maturing RGCs was examined. These included RGCs that exhibited either a transient, topographically incorrect, projection to the caudal superior colliculus (SC), or a transient projection to the caudal inferior colliculus (IC), in addition to a control group that exhibited a topographically correct projection to the caudal SC. Projection populations were identified by retrograde transport of rhodamine labeled latex microspheres injected into target nuclei. Labeled RGCs were then injected in vitro with Lucifer yellow to reveal the details of their dendritic morphology. Retinal ganglion cells making target errors, most of which ultimately die, were found to undergo a remarkable degree of morphological differentiation and could be categorized according to the adult type I, II, or III criteria. However, the relative proportions of these cell types were different among RGCs making transient connections versus those whose projections were preserved. Approximately half of the RGCs making topographically incorrect projections to the SC belonged to type III, in contrast to 6% that made a topographically correct projection. In addition, the population of cells sending axons to caudal IC did not include type III RGCs, but consisted of small type II neurons. The development of the basic dendritic form of each RGC type was only modestly influenced by its projection pattern; dendritic trees of cells making transient projections were essentially normal with only a slight, but statistically significant, reduction in dimensions. Moreover, dendritic remodeling was evident during maturation of neurons making either transient or normal projections. Together, these findings indicate that target specificity plays a relatively minor role on dendritic development of retinal ganglion cells.

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Brainstem inputs to the ferret medial geniculate nucleus and the effect of early deafferentation on novel retinal projections to the auditory thalamus

1998

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Following specific neonatal brain lesions in rodents and ferrets, retinal axons have been induced to innervate the medial geniculate nucleus (MGN). Previous studies have suggested that reduction of normal retinal targets along with deafferentation of the MGN are two concurrent factors required for the induction of novel retino-MGN projections. We have examined, in ferrets, the relative influence of these two factors on the extent of the novel retinal projection. We first characterized the inputs to the normal MGN, and the most effective combination of neonatal lesions to deafferent this nucleus, by injecting retrograde tracers into the MGN of normal and neonatally operated adult ferrets, respectively. In a second group of experiments, newborn ferrets received different combinations of lesions of normal retinal targets and MGN afferents. The resulting extent of retino-MGN projections was estimated for each case at adulthood, by using intraocular injections of anterograde tracers. We found that the extent of retino-MGN projections correlates well with the extent of MGN deafferentation, but not with extent of removal of normal retinal targets. Indeed, the presence of at least some normal retinal targets seems necessary for the formation of retino-MGN connections. The diameters of retino-MGN axons suggest that more than one type of retinal ganglion cells innervate the MGN under a lesion paradigm that spares the visual cortex and lateral geniculate nucleus. We also found that, after extensive deafferentation of MGN, other axonal systems in addition to retinal axons project ectopically to the MGN. These data are consistent with the idea that ectopic retino-MGN projections develop by sprouting of axon collaterals in response to signals arising from the deafferented nucleus, and that these axons compete with other sets of axons for terminal space in the MGN.

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Retinal ganglion beta cells project transiently to the superior colliculus during development.

Cited by 32 publications

References 28 publications

Stages of growth of hamster retinofugal axons: implications for developing axonal pathways with multiple targets

Stages of growth of hamster retinofugal axons: implications for developing axonal pathways with multiple targets

Transient retinal ganglion cells in the developing rat are characterized by specific morphological properties

Brainstem inputs to the ferret medial geniculate nucleus and the effect of early deafferentation on novel retinal projections to the auditory thalamus

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