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We investigated the morphological features of long range intrinsically projecting neurons and their pattern of axonal arborization in cat area 17 at different stages of postnatal development. In one set of experiments intracortically projecting cells were retrogradely labeled in vivo with rhodamine latex beads and then visualized by in vitro filling with Lucifer yellow. In another approach, intracortical fibers including the cells of origin were labeled postmortem in fixed brains with the lipophilic carbocyanine dye Dil. The results of this study indicate that the long-range intrinsic circuitry of the primary visual cortex develops in three major steps. The first step consists of the development of unclustered long-range axons in the two outer compartments of the cerebral cortex, layer I and the subplate. These early connections could serve as a scaffold for the organization of the tangential architecture of the neocortex as they originate from cells that are the first to receive synaptic input from extrinsic afferents. The second step consists of the outgrowth of horizontal axon collaterals originating from cells located in layers II-VI. During the first 2-3 weeks these connections still differ from those in the adult because they span shorter distances, originate more often from neurons with morphological features of nonpyramidal cells, and lack the precise clustering of the mature connections. The third step consists of a selection process that leads to the elimination of axon terminals from locations between the clusters of tangentially projecting neurons. This selection starts at the end of the second postnatal week and, hence, overlaps in time with the still proceeding elongation of axons and continues beyond the end of the fourth postnatal week when axon length has reached its maximal extent. This refinement process enhances the specificity of long-range connections and is probably influenced by visual experience.

The Origin and Topography of Long-Range Intrinsic Projections in Cat Visual Cortex: A Developmental Study