Postnatal development of axosomatic synapses in the rat visual cortex: Morphogenesis and quantitative evaluation

Abstract

Postnatal development of axosomatic synapses was studied in the rat visual cortex in order to obtain experimental data that may explain how the unequal distribution of asymmetric and symmetric synapses evolves on the soma of cortical neurons. Three types of synaptic junctions were identified: (1) asymmetric or type 1 synapses, with postsynaptic densities ≥ 20 nm, (2) symmetric type 2 synapses, and (3) symmetric synapses with an intermediate structure. The third synapse type had a structure similar to that of type 1 synapses, although the postsynaptic densities were thinner than 20 nm. Type 1 synapses developed in three phases. In phase 1, the first postnatal week, there were many free postsynaptic thickenings and immature synapses whereby a higher degree of postsynaptic differentiation was visible in comparison to the presynaptic elements. During the following 10 days, phase 2, type 1 synapses containing thin postsynaptic densities and intermediate synapses temporarily increased in number. Intermediate synapses are interpreted as precursors of type 1 synapses that have relatively immature postsynaptic elements. Toward the end of synaptogenesis, phase 3, the free postsynaptic thickenings reappeared while type 1 synapses containing well developed postsynaptic elements prevailed. Throughout the whole postnatal period, the numerical density of axosomatic type 1 synapses remained very low and the ratio of asymmetric to symmetric synapses at the neuronal somata was inversely proportional to that at the dendrites. Also, there was a significant decrease in the numerical density of type 1 synapses between postnatal days (P) 17 and 30. Data normalized according to cortical growth suggest that this is probably due to a decrease in the number of axosomatic type 1 synapses. This corresponds to the observation that in layers III and V a few type 1 synapses were found on pyramid‐like cells up to P10 which then disappeared in later stages. Axosomatic type 2 synapses appear to be formed by two different presynaptic processes. The first presynaptic type contains flocculent material with glycogen granules and resembles axonal growth cones. These junctions contain multiple adhesion patches, intermediate junctions, one or more active zones, narrow synaptic clefts, and small pleomorphic vesicles. All of these are structural features of adult type 2 synapses. The growth‐cone‐like presynaptic elements disappeared after about 3 weeks. The second presynaptic type is smaller in size and also forms contacts with a structure similar to adult type 2 synapses. During the first postnatal week, the numerical density of symmetrical synapses (including intermediate synapses) was very low and increased more or less at a regular pace until P55. These data suggest that during postnatal development fewer type 1 synapses are formed on the somata than in the surrounding neuropil, and there was an additional reduction in the number of axosomatic type 1 synapses during the third and fourth postnatal week.