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

Abstract

SUMMARY1. 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 ofthe 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 gm 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 laminae 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.

Regulation of retinal ganglion cell axon arbor size by target availability: Mechanisms of compression and expansion of the retinotectal projection

“…11). Axons in enucleates spread extensively over the collicular surface but restrict the depth of their arborization with respect to the collicular surface, which has been observed in prior anatomical and physiological studies (Finlay et al, 1979b;Rhoades, 1980;Thompson, 1979). Thus, the mean area occupied by the ENUC arbors is significantly larger than normal for the retinotopic plane by covering a mean area of 106,000 ?…”

“…The area of arbors in this plane is 45,000 * 1,600 pm2. This preference for occupation of the dorsal aspect of the SC in both depleted or "compressed" projections has been noted in several other contexts (Finlay et al, 1979a,b;Finlay, 1979;Rhoades, 1980;Thompson, 1979). Because we found no difference in area comparing normal and neonatal-IPS1 axons for the retinotopic plane, we did not explore the difference of neonatal-IPS1 and normal-IPS1 in the axon entry plane.…”

“…The anomalous ipsilateral projection of the remaining eye forms an expanded, functional projection in the colliculus compared with the normal ipsilateral projection (Finlay et al, 1979b;Thompson, 1979;Rhoades, 1980). Receptive fields in this projection are abnormally large and habituate rapidly, and responding cells are most likely to be found in the upper half of the superficial grey layer.…”

“…Monocular enucleation in hamster is a good model for this question. Neonatal removal of one eye in hamster results in the loss of the normal massive contralateral projection to the superior colliculus and an increased ipsilateral projection from the remaining eye, which is due to both sprouting of the ipsilateral projection in the temporal retina and also to a stabilized, exuberant projection from the contralateral nasal retina (Finlay et al, 1979a;Rhoades, 1980;Sengelaub et al, 1983;Thompson, 1979). Even with the increase in volume of the ipsilateral projection, retinal synaptic density is reduced in the tectum (Xiong and Finlay, 1993).…”

Plasticity in the superior collicular auditory space map of adult guinea‐pigs

“…Knudsen, 1988;King & Moore, 1991). Visual deprivation has been demonstrated to increase the number and distribution of auditory-responsive cells in the SC (Rhoades, 1980;King, 1990). Moreover, perturbation of visual experience during development results in disruption of auditory spatial properties of superior collicular neurones (King et al 1988;Knudsen, 1988;Withington-Wray et al 1990 …”