Effects of neonatal enucleation on the functional organization of the superior colliculus in the golden hamster.

1. The responses of visual, auditory and somatosensory superior collicular neurones were investigated using extracellular single unit recording techniques in hamsters which were subjected to the removal of one eye on the day of birth. 2. Neonatal enucleation resulted in a marked increase in the region of the colliculus from which visual neurones activated by stimulation of the ipsilateral eye could be recorded. In most cases the visuotopic representation in the colliculus ipsilateral to the remaining eye mirrored that observed in the contralateral tectum along both the rostrocaudal and mediolateral axes: in both colliculi temporal retina projected rostrally and inferior retina medially. In some animals, however, there appeared to be a dual mapping of the remaining eye onto the ipsilateral tectum. In these hamsters the central portion of the visual field was represented twice along the rostrocaudal axis of colliculus. 3. No changes in the topography of the somatosensory and auditory representations in the tectum were observed following neonatal enucleation. 4. The laminar distribution of visual neurones in the ipsilateral colliculus was markedly altered in the neonatally enucleated hamsters. Very few exclusively visual units were encountered in the layers ventral to the stratum opticum and almost all of the visual cells recorded in the ipsilateral colliculus were isolated within 150 microM of the tectal surface. 5. In the posterior half of the ipsilateral tectum a large number of extravisually responsive cells were encountered in the stratum griseum superficiale and stratum opticum. This was not the case in the colliculus contralateral to the remaining eye, nor has it ever been observed in normal hamsters. 6. Recordings from animals subjected to both neonatal enucleation and acute bilateral removal of somatosensory and auditory cortex indicated that the projections from these areas to the colliculus were not essential to the observed changes in laminar organization. 7. Recordings from normally reared hamsters which were subjected to removal of one eye at the time of the recording experiment suggested further that the isolation of extravisual cells in the superficial tectal aminae of the neonatal enucleates was probably not the result of the 'unmasking' of extravisual influences in the superficial layers which are present, but ineffective, in the normal case.