Tempo of neurogenesis and synaptogenesis in the primate cingulate mesocortex: Comparison with the neocortex

Abstract
In the neocortex, the onset of the rapid phase (phase 3) of synaptogenesis occurs after the end of neurogenesis. However, we still do not know whether or not these two developmental events are causally related. The present study compares the time-course and tempo of neurogenesis and synaptogenesis in the anterior cingulate cortex (area 24 of Brodmann) and in the primary visual cortex (area 17) in a series of pre- and postnatal rhesus monkeys. Autoradiographic analysis of animals fetally injected with 3H-thymidine showed that all neurons destined for area 24 are generated by embryonic day 70, which is 30 days earlier than in area 17. The rapid phase of synaptogenesis in area 24 starts during the third embryonic month and continues at the same rate through the remainder of gestation and the first 2 months after birth, as has been seen in neocortical areas examined previously. Statistical analysis of the linear portions of the rapid phase indicates that, although neurogenesis in area 24 is completed 1 month earlier than in area 17, the rapid phase of synaptogenesis occurs 41 days later. Moreover, the tempo of synaptic accretion was remarkably similar to that in motor, somatosensory, visual, or associational areas. All were grouped within the same time window of about 40 days, centered at birth. After the second postnatal month, synaptic density in area 24 remains at a high level until sexual maturity. This work shows that the rapid phase of synaptogenesis in the cingulate mesocortex is not linked temporally to the end of neurogenesis. We suggest that it is regulated by the same genetic or humoral factors that control synaptogenesis in the phylogenetically newer neocortical areas.