Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage.

The kinetics of synaptogenesis in the primary visual cortex (Brodmann's area 17) were analyzed by electron microscopy in 33 rhesus monkeys, ranging in age from the 50th embryonic day (E50) to 20 years. A series of overlapping electron micrographs (vertical probes) were examined at each age on sections of the upper bank of the calcarine fissure. Synaptic contacts were first observed in the E50 specimen in the subplate and marginal zone (prospective layer I). In the cortical plate itself, synapses appear between E65 and E89 starting in the prospective layer VI. By E112, after all cortical neurons have assumed their laminar positions, synapses situated predominantly on dendritic shafts were present at a low density throughout the full thickness of the cortical plate. Thereafter, synapses accumulate more rapidly on dendritic spines and by E144 an equal number of contacts are found on both spines and shafts. The density of synapses continues to increase exponentially in all layers and reaches the mean maximum density of about 90 synapses per 100 microns 3 of neuropil by the third postnatal month. During the next 2 postnatal years the density of synaptic contacts decreases only slightly to a mean of 80/100 microns 3 of neuropil. Around the time of puberty, however, synaptic density decreases more rapidly to reach the adult level of about 40-50/100 microns 3 of neuropil. The 40% decrease in the density of synaptic contacts occurring between 2.7 and 5 years represents a loss of about 5000 synapses per second in the primary visual cortex of the two hemispheres, due primarily to the loss of asymmetric synapses situated on dendritic spines. The transient phase of high density of synaptic contacts located on dendrospines is shorter in thalamo-recipient layer IV than in either supra- or intragranular layers and is completed within the first postnatal year. It ends earlier in sublayer IVC than in layers IVAB and II-III, for example, reflecting biochemical and functional maturation of the different visual subsystems.