Polyribosomes under developing spine synapses: growth specializations of dendrites at sites of synaptogenesis

We have previously reported that there is a dramatic increase in polyribosomes associated with dendritic spines during periods of synapse growth induced by denervating lesions. We suggested that polyribosomes at the postsynaptic site may somehow be involved in the growth of synapses. To evaluate this hypothesis further, the present study determines whether synapses which are growing in the developmental period also have accumulations of polyribosomes. We examined the dentate gyrus of the developing rat electron microscopically at 7, 10, 15, 20, and 28 days of age, which spans the major period of synaptogenesis in this structure. Qualitative observations revealed dramatic accumulations of polyribosomes under spine synapses in the youngest animals (7 and 10 days of age). With synapse development, the accumulations of polyribosomes became less dramatic, so that by 28 days of age, the neuropil of the dentate gyrus appeared qualitatively mature. To determine the relationship between polyribosomes under spine synapses and synapse development, quantitative electron microscopic methods were use to evaluate synapse density (number of synapses/100 micron 2), and the incidence of polyribosome-containing spines (proportion of spine synapses with underlying polyribosomes) in the neuropil of the dorsal blade of the dentate gyrus at each age. An inverse relationship was found between synapse density and the proportion of spines with polyribosomes. Synapse density increased in an almost linear fashion between 7 and 28 days of age to levels which were actually somewhat higher than in mature rats, whereas the incidence of polyribosome-containing spines was highest at the youngest ages and decreased with development. Thus, polyribosomes were most prominent under spine synapses during the period of maximal synapse growth. These results, together with our previous observations of increased numbers of polyribosomes under spines during lesion-induced growth, suggest that the polyribosomes represent a structural specialization of dendrites at sites of synapse construction. We propose that they produce protein(s) that are involved in synapse growth.