Intrinsic determinants of retinal axon collateralization and arborization patterns

Permanent, novel retinal projections to the principal thalamic somatosensory (ventrobasal) or auditory (medial geniculate) nuclei can be produced in adult hamsters if the superior colliculus is ablated bilaterally and the somatosensory and auditory lemniscal axons are transected unilaterally on the day of birth. We studied the development of those novel projections by labeling retinal axons with the fluorescent tracer 1,1'-dioctadecyl-3,3,3', 3'-tetramethylindocarbocyanine perchlorate to examine the relative roles of intrinsic factors and axon-target interactions in the specification of retinal axon connections. Our principal findings are as follows: (1) In hamsters operated on the day of birth to produce the novel retinal projections, retinal ganglion cell axons projecting to the ventrobasal or medial geniculate nuclei develop in three morphologically distinct stages, i.e., elongation, collateralization, and arborization, as do retinal axons projecting to the dorsal lateral geniculate nucleus, the principal thalamic visual nucleus, in normal hamsters. (2) In both the ventrobasal and medial geniculate nuclei of operated hamsters, as in the dorsal lateral geniculate nucleus of normal hamsters, collateral branches were initially formed by retinal ganglion cell axons in both the superficial and internal components of the optic tract and only collaterals from the superficial component formed permanent projections. (3) The retinofugal axon terminal arbors in the ventrobasal and medial geniculate nuclei of mature, operated hamsters resemble the same three morphologic classes that are observed in the lateral geniculate nucleus of normal hamsters, although their absolute size appears to be altered. These data suggest that both superficial and internal optic tract axons can produce thalamic collaterals during development but that only superficial optic tract axons can permanently retain thalamic collaterals. Furthermore, the same morphologic types of retinofugal axons appear to contribute to normal and surgically induced retinal projections.