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Developing binocular projections to the Xenopus tectum require visual input in order to establish matching topographic maps. In dark-reared Xenopus, the ipsilateral eye's map, relayed via the retino-tecto-isthmotectal pathway, fails initially to acquire normal rostrocaudal order. Moreover, with extended time in the dark, the ipsilateral map becomes progressively less well organized. This phenomenon showed that without binocular cues, the isthmotectal axons are unable to locate proper sites for their terminal zones but left open the issue of whether the axons are able to establish arbors of normal dimensions and/or to sustain normal numbers of branches. In order to test whether dark-rearing modifies isthmotectal axon branching, we have used horseradish peroxidase to examine axons of Xenopus after dark-rearing for periods from 3 to 298 weeks. The results demonstrate that these axons never acquire more than about half the normal numbers of terminals. Surprisingly, however, the dark-reared axons' terminal zones are normal in mediolateral and rostrocaudal extent despite the lack of binocular cues that normally could constrain arbor size by inducing pruning of branches in regions with mismatched visual inputs. The effects of dark-rearing are reversible. After a return to normal lighting conditions, the recovery process begins quickly, with a significant increase in branch numbers within 4 weeks. The terminal zone remains of normal dimensions. These results support the hypothesis that correlated binocular visual input is essential for the maintenance of normal numbers of isthmotectal branches but that normal termination zone size can be established in the absence of visual cues.

During the development of binocular maps in the tectum of Xenopus laevis, axons that relay input from the ipsilateral eye via the nucleus isthmi undergo a prolonged period of shifting connections. This shifting accompanies the dramatic change in eye position that takes place as the laterally placed eyes of the tadpole move dorsofrontally. There is a concomitant expansion of the proportion of tectum that receives contralateral retinotectal input corresponding to the binocular portion of the visual field. Electrophysiological recording demonstrates that ipsilateral units are present in those rostral tectal zones, and anatomical methods show that the isthmotectal axons arborize densely in the rostral region but also extend sparser branches into the caudal zone, which is occupied by contralateral inputs with receptive fields in the monocular zone of the visual field. A mechanism that aligns the ipsilateral and contralateral maps is activity-dependent stabilization of isthmotectal axons that exhibit firing patterns correlated with those of nearby retinotectal axons. In order for activity patterns to function in stabilizing correct connections and promoting the withdrawal of incorrect connections, synaptic communication of some sort is hypothesized to be essential. We have investigated whether isthmotectal axons make morphologically identifiable synapses during development and where such synapses are located. We find evidence for morphologically identifiable synapses in all regions of the tectum, along with many growth cones and structures that are probably immature synapses. As in the adult, the synapses contain round, clear vesicles, have asymmetric specializations, and terminate on structures that appear to be dendrites. In both adult and tadpole, the rarity of serial synapses involving isthmotectal terminals suggests that the interactions between retinotectal and isthmotectal inputs are mediated by postsynaptic dendrites.

The connections between the nucleus isthmi and the tectum in the frog have been determined by several anatomical techniques: iontophoresis of horseradish peroxidase into the tectum, iontophoresis of 3H-porline into the nucleus isthmi and the tectum, and Fink-Heimer degeneration staining after lesions of the nucleus isthmi. The results show that the nucleus isthmi projects bilaterally to the tectal lobes. The ipsilateral isthmio-tectal fibers are distributed in the superficial layers of the tectum, coincident with the retionotectal terminals. The contralateral isthmio-tectal fibers travel anteriorly adjacent to the lateral optic tract and cross the midline in the supraoptic ventral decussation, where they turn dorsally and caudally; upon reaching the tectum, the fibers end in two discrete layers, layers 8 and A of Potter. The tectum projects to the ipsilateral nucleus isthmi and there is a reciprocal topographic relationship between the two structures. Thus, a retino-tecto-isthmio-tectal route exists which may contribute to the indirect ipsilateral retinotectal projection which is observed electrophysiologically. The connections between the nucleus isthmi and the tectum in the frog are strinkingly similar to the connections between the parabigeminal nucleus and the superior colliculus of mammals.

In this paper we present evidence that early eye rotation in Xenopus leads to anatomical rearrangements in a portion of the binocular visual system. In the past, electrophysiological mapping had shown that the topography of the ipsilateral visuotectal projection is changed by such eye rotation and that this change requires visual experience. However, knowledge of the anatomical basis for this electrophysiological change was lacking. The identification of the nucleus isthmi as a link in the projection has allowed us to study the topography of the ipsilateral system by use of horseradish peroxidase. We present data showing that early eye rotation alters the topography of the crossed isthmotectal projection. These results demonstrate that the orientation of a topographically organized projection can be changed by procedures which do not involve direct manipulation of the source, pathway, or target of the projection.