The principle of "conservation of total axonal arborizations": massive compensatory sprouting in the hamster subcortical visual system after early tectal lesions

Unilateral lesions of the right superior colliculus (SC) were made in hamsters on the day after birth. In order to quantify the extent of abnormal innervation by left eye fibers in the diencephalon and midbrain, the left eye was removed on postnatal day 12 or 36, and after an appropriate survival time, the brains were stained for degenerating axons and axon terminals with the Fink-Heimer method. In additional cases, anterograde transport of 3H proline-leucine or horseradish peroxidase was used to assess left eye connectivity. In agreement with previous reports we found abnormal projections in the ventral nucleus of the lateral geniculate body (LGv), in the lateral posterior nucleus (LP) of the thalamus, and in the left SC (the 'recrossing' pathway). We also noted areas of abnormally heavy terminal fields arranged in patches in coronal sections in the dorsal nucleus of the lateral geniculate body (LGd). These patches arise from columns of dense innervation that are oriented along a rostral-to-caudal axis. If the right SC lesion was made large enough to diminish the recrossing pathway, retinofugal axons establish a significantly smaller distal terminal field in the left SC. In these cases, a corresponding increase in the size of terminal fields in all major proximal structures (LGd, LGv, LP, DTN) was observed. The sum of abnormal proximal growth ("compensatory sprouting") was found to truly compensate for the distal loss of terminals. The evaluation of hamsters in which left eye connectivity was assessed at the age of 12 days revealed that lesion-induced patches of abnormal growth have already reached their full size by that time. These findings provide evidence for the 'pruning-effect' and demonstrate that retinofugal axons support a fixed number of terminal arborizations (the principle of 'conservation of total axonal arborizations').