Developmental remodeling of primate visual cortical pathways.

Abstract

The pre- and postnatal developmental changes of the cortical afferents to area 17 were studied in the macaque monkey. Paired injections of the retrograde tracers fast blue and diamidino yellow were made in area 17. Quantitative techniques were used to examine the spatial patterns of labeling in three distinct locations of the extrastriate cortex that correspond to known visual areas. In the adult, each cortical region has a characteristic laminar distribution. In the fetus the proportion of supragranular layer neurons in all cortical regions was much higher than in the adult. The present study shows that despite the very high levels of labeled supragranular layer neurons, there is some early areal specialization so that the adult configuration does not emerge from a uniform distribution. The developmental decline in the proportion of labeled supragranular neurons is complete by 1 month after birth. Each injection of tracer gave rise in each cortical area to dense labeling in a restricted region (projection zone). Areal measurements of projection zones in the supra- and infragranular layers showed that the developmental decrease in the proportion of labeled supragranular layer neurons is accompanied by a relative change of the dimensions of supra- and infragranular projection zones: the supragranular projection zone in the fetus is larger than the infragranular projection zone and vice versa in the adult. In the fetus, the two projection zones corresponding to each of the two tracers overlap in the supragranular layers whereas they are largely separated in the infragranular layers. During development there is a progressive decrease in the overlap of the supragranular projection zones and an increase in the overlap in the infragranular layers. Again, the adult configuration is achieved 1 month after birth. This developmental inversion of the areal dimensions of the projection zones in supra- and infragranular layers is accompanied by a drastic decrease in the proportion of double-labeled neurons located in supragranular layers. These results clearly show that early in development, axonal projections to area V1 are modified in very different ways according to whether they originate from supra- or infragranular layers. This developmental process lasts for about 80 d. These findings show that in the primate there is a prolonged remodeling of axonal projections that is a highly characteristic feature of this species.