The role of visual experience in the formation of binocular projections in frogs
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Many parts of the visual system contain topographic maps of the visual field. In such structures, the binocular portion of the visual field is generally represented by overlapping, matching projections relayed from the two eyes. One of the developmental factors which helps to bring the maps from the two eyes into register is visual input.
The role of visual input is especially dramatic in the frog,Xenopus laevis. In tadpoles of this species, the eyes initially face laterally and have essentially no binocular overlap. At metamorphosis, the eyes begin to move rostrodorsally; eventually, their visual fields have a 170° region of binocular overlap. Despite this major change in binocular overlap, the maps from the ipsilateral and contralateral eyes to the optic tectum normally remain in register throughout development.
This coordination of the two projections is disrupted by visual deprivation. In dark-rearedXenopus, the contralateral projection is nearly normal but the ipsilateral map is highly disorganized.
The impact of visual input on the ipsilateral map also is shown by the effect of early rotation of one eye. Examination of the tectal lobe contralateral to the rotated eye reveals that both the contralateral and the ipsilateral maps to that tectum are rotated, even though the ipsilateral map originates from the normal eye. Thus, the ipsilateral map has changed orientation to remain in register with the contralateral map. Similarly, the two maps on the other tectal lobe are in register; in this case, both projections are normally oriented even though the ipsilateral map is from the rotated eye.
The discovery that the ipsilateral eye's map reaches the tectum indirectly, via a relay in the nucleus isthmi, has made it possible to study the anatomical changes underlying visually dependent plasticity. Retrograde and anterograde tracing with horseradish peroxidase have shown that eye rotation causes isthmotectal axons to follow abnormal trajectories. An axon's route first goes toward the tectal site where it normally would arborize but then changes direction to reach a new tectal site. Such rearrangements bring the isthmotectal axons into proximity with retinotectal axons which have the same receptive fields.
Anterograde horseradish peroxidase filling has also been used to study the trajectories and arborizations of developing isthmotectal axons. The results show that the axons enter the tectum before the onset of eye migration but do not begin to branch profusely until eye movement begins to create a zone of binocular space. Throughout the period of greatest eye movement, many isthmotectal arbors are larger and more diffuse than in older animals.
A proposal, based on the Hebb-synapse model, is offered to explain how interactions of isthmotectal axons with other isthmotectal axons and with retinotectal axons could help to organize the ipsilateral map and bring it into alignment with the contralateral map.
Key wordsfrogs nucleus isthmi development visual experience tectum
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