Development of gemculocortical projections to visual cortex in rat: Evidence for early lngrowth and synaptogenesis

Abstract

Anterograde movement of Dil and transneuronal transport of wheat germ aghitinin-horseradish peroxidase (WGA-HRP) were used to study the temporal and laminar patterns of ingrowth of the geniculocortical projection to visual cortex in fetal and postnatal rats. The development of this projection was compared to patterns of migration and settling of L HJ-thymidine-labeie neurons destined for cortical layer IV, and to geniculocortical synapse formation. Dil-labeied geniculocortical axons were found in the intermediate zone beneath the lateral cerebral mantle at embryonic day (E) 17 and in the subplate layer underlying visual cortex by EIS. On E 19 they appeared to accumulate and grow radially into an expanding subplate layer and into the deep part ofdeveloping cortical layer VI. By postnatal day (P)0, Dil or WGA-HRP-labeled geniculocortical axons were found in developing cortical layers VI and V. By P l, they invaded the deep portion ofthe cell-dense cortical plate, where they were in position to make initial contact with neurons that would later form layer IV. A few xons traversed the cortical plate to reach the marginal zone. Layer IV became an identifiable layer on P2, and s clear projection to layer IV was evident by P3. These results suggest that geniculocortical afferents grow continuously from the intermediate zone, initially into an expanding subplatt layer and then sequentially into each of the developing cortical layers without evidence of “waiting”. Electron microscopic data suggest that geniculocortical axons begin to form immature synapses with dendrites and neuronal perikaryas they first encounter cortical neurons, first in the subplate layer and then in developing layers VI, V and marginal zone, in addition to the primary target layer IV. The precise targetmg and overall temporal and laminar patterns of ingrowth and synaptogenesis suggest that geniculocortical axons are directed to the visual cortex by guidance cues within the internal capsule and subplate. Further, they reach the occipital pole early enough to influence the specification and histogenesis of cortical area 17, perhaps by exerting an influence on the deep-to-superficial “wave” of neuronal differentiation in sequentially developing subplate and cortical layers VI, V and IV.