Effects of very early monocular and binocular enucleation on primary visual centers in the tammar wallaby (Macropus eugenii)

The role of retinal afferents and their binocular interactions in the development of mammalian primary visual centers has been studied in the marsupial wallaby. Monocular and binocular enucleation was performed prior to any retinal innervation of the visual centers. After monocular enucleation retinal projections were traced by horseradish peroxidase histochemistry and compared with those in normal animals and those during development. The topography of retinal projections to the superior colliculus and the dorsal lateral geniculate nucleus after monocular enucleation was determined by making retinal lesions and tracing the remaining projections with horseradish peroxidase. The position and nature of the filling defects in terminal label were compared with controls with similarly placed lesions. The superior colliculus and dorsal lateral geniculate nucleus ipsilateral to the remaining eye were shrunken. Projections to the ipsilateral superior colliculus, ipsilateral accessory optic nuclei, and ipsilateral suprachiasmatic nucleus, although enlarged, never approached the density contralaterally, as was also the case during normal development. The expanded projection in the ipsilateral superior colliculus came primarily from temporal and ventral retina. In the dorsal lateral geniculate nucleus, terminal bands and cellular laminae, although not identical to normal, did develop. During normal development overlap of afferents from the two eyes occurs in the binocular region. The decrease in volume of the nucleus ipsilateral to the remaining eye after monocular enucleation suggests that the monocular region disappears in the absence of appropriate input and the binocular region survives. Contralaterally there was no decrease in volume, compatible with this idea. The topography of retinal projections supports this interpretation. It was normal contralaterally while ipsilaterally it was appropriate for the normal binocular region. There was an expansion of the projection along the lines of projection in what would normally be binocular regions of the nucleus, where retinal afferents failed to segregate in the absence of binocular competition. After binocular enucleation the alpha and beta segments of the dorsal lateral geniculate nucleus were still recognizable but cell-sparse zones were absent, as was the characteristic orientation of primary dendrites of geniculocortical cells. There are rigid developmental constraints operating on the innervation of territory by retinal afferents from the two eyes, and many features of the mature pattern arise without binocular interactions during development.