Anatomical mapping of retino-tectal connections in developing and metamorphosed Xenopus: evidence for changing connections

Development ◽  
1978 ◽  
Vol 45 (1) ◽  
pp. 249-270
Author(s):  
Alison Longley

Neural connections between the eye and optic tectum in Xenopus laevis were anatomically traced by observing the tectal location of Wallerian degeneration after discrete retinal lesion. These retinotectal connections were mapped in postmetamorphic frogs and tadpoles at stage 51, the stage at which retinal axons have grown into about the rostral one-half of the tectum. The course of the experimental degeneration was the same in frogs and tadpoles, but degeneration proceeded faster in the younger animals. In the frogs, connections were ordered, with nasal retina mapping to the caudal part of the tectum and temporal retina mapping to the rostral tectum. In the tadpoles, within the innervated area at the rostral tectum, the retino-tectal connections were generally organized as in the adults, with the temporal retina mapping to the rostral part of the innervated tectum and nasal retina mapping primarily to the caudal part. But a portion of the nasal fibers consistently mapped to the far rostral tectum as well. Electron microscopic observations showed degenerating synaptic terminals at both rostral and caudal portions of the innervated tectum after lesion of just the nasal retina. Degeneration was not seen in control animals. These results indicate that some fibers (particularly from nasal retina) may shift their terminals caudally on the tectum to match tectal growth and produce the adult pattern of connections. If there is such connection readjustment, the ‘aberrant’ connections from nasal retina in tadpoles may be an indication of this process.

Development ◽  
1990 ◽  
Vol 110 (2) ◽  
pp. 331-342 ◽  
Author(s):  
H. Ichijo ◽  
S. Fujita ◽  
T. Matsuno ◽  
H. Nakamura

Retinotectal projection is precisely organized in a retinotopic manner. In normal projection, temporal retinal axons project to the rostral part of the tectum, and nasal axons to the caudal part of the tectum. The two-dimensional relationship between the retina and the tectum offers a useful experimental system for analysis of neuronal target recognition. We carried out rotation of the tectal primordium in birds at an early stage of development, around the 10-somite stage, to achieve a better understanding of the characteristics of target recognition, especially the rostrocaudal specificity of the tectum. Our results showed that temporal retinal axons projected to the rostral part of the rotated tectum, which was originally caudal, and that nasal axons projected to the caudal part of the rotated tectum, which was originally rostral. Therefore, the tectum that had been rotated at the 10-somite stage received normal topographic projection from the retinal ganglion cells. Rostrocaudal specificity of the tectum for target recognition is not determined by the 10-somite stage and is acquired through interactions between the tectal primordium and its surrounding structures.


1990 ◽  
Vol 4 (6) ◽  
pp. 519-531 ◽  
Author(s):  
Thomas E. Hughes

AbstractThe superficial layers of the frog's optic tectum, Potter's (1969) layers A-G, comprise a complex neuropil made up of many afferent axons, the somata of a few neurons, and many dendrites from the neurons located in the deeper layers. Different types of retinal axons are believed to terminate in different layers (Maturana et al., 1960; Kuljis & Karten, 1988; Sargent et al., 1989), but little is known about the relationships between each type of input and the dendrites of the deep tectal neurons that extend into these superficial layers. The present study used the method of retrograde transport of horseradish peroxidase to study the synaptic contacts on the dendrites of the neurons that give rise to the crossed tecto-bulbar pathway. These cells have apical dendrites that ascend through the superficial retino-recipient layers.The somata of the cells that give rise to the crossed tecto-bulbar pathway are located in the superficial half of layer 6, preferentially clustered along the caudal, lateral, and rostral margins of the tectum. The somata of these cells range from 8−30 ¼m in diameter. Their axons are large (2−4 ¼m in diameter) myelinated fibers that arise from either their somata or proximal dendrites. Their axons travel within the deep medullary layer to leave the tectum at the lateral margin. Their dendritic arbors extend obliquely through the superficial layers to reach layer B where they turn and extend within the layer for up to 0.5 mm. The somata of these cells receive only a scant synaptic input. In contrast, their dendrites receive input in every layer, but the nature of this input varies from layer to layer. Synaptic terminals that resemble retinal ganglion cell boutons contact the labeled dendrites in layers B, F, and G. This indicates that the dendrites may receive monosynaptic input from several types of retinal ganglion cells. Terminals with small, flattened vesicles also contact the dendrites of these cells in each layer. In layer F and below, the terminals with flattened vesicles constitute 15% of the contacts; above layer F they constitute only 5−8% of the contacts. Terminals with medium-sized, flattened vesicles also contact the dendrites of these cells in every layer and constitute a large proportion of their input (33−95%). The latter terminals resemble those that are often postsynaptic to retinal terminals.


1990 ◽  
Vol 4 (6) ◽  
pp. 499-518 ◽  
Author(s):  
Thomas E. Hughes

AbstractThere are several different groups of ganglion cells in the retina of the frog. Although their axons are thought to terminate in different layers of the optic tectum, little is known about the morphology of their terminal arbors or their synaptic targets. The present paper reports the results of a layer-by-layer study of horseradish peroxidase labeled retinal axons in the optic tectum of Rana pipiens. Light and electron microscopy was used to study the axon's laminar distribution, patterns of arborization, and synaptic contacts.Labeled retinal axons were found in all of the superficial layers of the tectum (A-G). From layer to layer, the retinal axons differed markedly in the diameter of their parent axons (0.2−3.0 μm) and in the morphology and horizontal extent of their terminal arbors.Five classes of synaptic terminals could be distinguished in the tectum. The retinal terminals belonged to class characterized by round, medium-sized synaptic vesicles. They made synaptic contact with dendrites and other axon terminals in each of the layers. They were always the presynaptic component. The postsynaptic dendrites were often the vertically oriented processes of cells located in the deeper layers. The postsynaptic terminals belonged to a class distinguished by their flat, medium-sized vesicles. These terminals in turn contacted what appeared to be dendrites. In layer eight, the retinal axons were often large, spoon-shaped boutons that ended in apposition with the somata of the layer.


1983 ◽  
Vol 41 (3) ◽  
pp. 215-227 ◽  
Author(s):  
Eros Abrantes Erhart ◽  
Ciro Ferreira da Silva ◽  
Claudio Fava Chagas

Electron microscopic findings on the nerve of the biventer cervicis muscle of the chick, which was completely transected and immediately after submitted to an adequate microsurgical nerve suture, confirmed our previous statement that proper microsurgical nerve suture may impede the Wallerian degeneration that normally occurs in the distal segment of a completely transected nerve.


1999 ◽  
Vol 81 (2) ◽  
pp. 895-907 ◽  
Author(s):  
James A. Edwards ◽  
Hollis T. Cline

Light-induced calcium influx into retinal axons is regulated by presynaptic nicotinic acetylcholine receptor activity in vivo. Visual activity is thought to be a critical factor in controlling the development of central retinal projections. Neuronal activity increases cytosolic calcium, which was hypothesized to regulate process outgrowth in neurons. We performed an in vivo imaging study in the retinotectal system of albino Xenopus laevis tadpoles with the fluorescent calcium indicator calcium green 1 dextran (CaGD) to test the role of calcium in regulating axon arbor development. We find that visual stimulus to the retina increased CaGD fluorescence intensity in retinal ganglion cell (RGC) axon arbors within the optic tectum and that branch additions to retinotectal axon arbors correlated with a local rise in calcium in the parent branch. We find three types of responses to visual stimulus, which roughly correlate with theon, off, and sustained response types of RGC reported by physiological criteria. Imaging in bandscan mode indicated that patterns of calcium transients were nonuniform throughout the axons. We tested whether the increase in calcium in the retinotectal axons required synaptic activity in the retina; intraocular application of tetrodotoxin (10 μM) or nifedipine (1 and 10 μM) blocked the stimulus-induced increase in RGC axonal fluorescence. A second series of pharmacological investigations was designed to determine the mechanism of the calcium elevation in the axon terminals within the optic tectum. Injection of bis-( o-aminophenoxy)- N, N, N′, N′-tetraacetic acid-AM (BAPTA-AM) (20 mM) into the tectal ventricle reduced axonal calcium levels, supporting the idea that visual stimulation increases axonal calcium. Injection of BAPTA (20 mM) into the tectal ventricle to chelate extracellular calcium also attenuated the calcium response to visual stimulation, indicating that calcium enters the axon from the extracellular medium. Caffeine (10 mM) caused a large increase in axonal calcium, indicating that intracellular stores contribute to the calcium signal. Presynaptic nicotinic acetylcholine receptors (nAChRs) may play a role in axon arbor development and the formation of the topographic retinotectal projection. Injection of nicotine (10 μM) into the tectal ventricle significantly elevated RGC axonal calcium levels, whereas application of the nAChR antagonist αBTX (100 nM) reduced the stimulus-evoked rise in RGC calcium fluorescence. These data suggest that light stimulus to the retina increases calcium in the axon terminal arbors through a mechanism that includes influx through nAChRs and amplification by calcium-induced calcium release from intracellular calcium stores. Such a mechanism may contribute to developmental plasticity of the retinotectal system by influencing both axon arbor elaboration and the strength of synaptic transmission.


1998 ◽  
Vol 15 (10) ◽  
pp. 853-906 ◽  
Author(s):  
Y Abe ◽  
T Yamamoto ◽  
Y Sugiyama ◽  
H Kayama ◽  
T Watanabe ◽  
...  

1989 ◽  
Vol 45 (1) ◽  
pp. 15-27 ◽  
Author(s):  
J. Vanselow ◽  
S. Thanos ◽  
P. Godement ◽  
S. Henke-Fahle ◽  
F. Bonhoeffer

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