Development of anomalous retinal projections to nonvisual thalamic nuclei in Syrian hamsters: a quantitative study

When two of the principal targets of retinofugal axons, the superior colliculus and dorsal nucleus of the lateral geniculate body, are ablated in newborn hamsters and the somatosensory (ventrobasal) or auditory (medial geniculate) thalamic nuclei are partially deafferented, the optic axons form permanent, abnormal connections in the latter nuclei. The lateral posterior nucleus of the operated hamsters also receives an anomalously large retinal projection. Here, we report on the results of a quantitative study that was undertaken in order to elucidate how these abnormal connections are formed. In normal, newborn hamsters, there is a transient retinal projection to the ventrobasal nucleus that disappears 3-4 days postnatally. Our quantitative data show that postoperatively, the volume of the retino-ventrobasal projection increases proportionately more than the volume of the ventrobasal nucleus so that the retino-ventrobasal projection in operated adult hamsters is due both to the stabilization of the normally transient projection and to a reactive sprouting that increases the size of the projection. The retino-medial geniculate projection arises de novo by reactive sprouting of optic tract fibers that normally pass over and through the nucleus; in unoperated hamsters, terminating projections are never seen at any age. The quantitative data also show that the anomalously large retino-lateral posterior projection is due almost entirely to the reactive sprouting of the normal projection and/or normal fibers of passage that are already present on the day of birth, although it is possible that a minor component can be attributed to the stabilization of a small population of normally transient retino-lateral posterior axons. The present results demonstrate that the transient retino-ventrobasal axons in normal, newborn hamsters are capable of making permanent connections with ventrobasal neurons. This finding raises the important question of the cellular mechanisms that determine whether immature neuronal connections are stabilized or eliminated. The results also suggest that during both normal and abnormal development, the choice of a target by growing axons may depend upon the axons being in proximity to a potential terminal site just at the time when that site is capable of receiving afferents.