The naturally occurring dynamics of presynaptic axon terminals were investigated in the dentate gyrus and stratum lucidum of the spiny mouse (Acomys cahirinus) during maturation, adulthood and aging. A sensitive and selective silver-staining technique was applied to analyze neuronal lysosome accumulation (LA), indicating synaptic degradation during development. LA was quantified by counting silver grains in the inner third and outer two thirds of the molecular layer, granular layer, and the infragranular layer of the dentate gyrus, and in the strata oriens, pyramidale, lucidum and radiatum of the medial and distal regio inferior on postnatal days 21, 28, 95, 730, and 1,460. In young and adult animals, LA was most abundant within the inner molecular layer. When animals grew older, LA densities obviously decreased in the inner molecular layer but increased in the outer molecular layer. Within the stratum lucidum only the distal regio inferior showed an extremely high LA density on postnatal day 21, dramatically decreasing thereafter and reaching adult low values during the first postnatal month. By electron microscopy in the inner molecular layer we found LA in large synaptic boutons and small terminals both with distinct synaptic contact zones. Degrading presynaptic profiles may further accumulate dense bodies, zones with completely disorganized cytoplasm, and lamellarly organized whorled membrane debris. In the distal regio inferior comparable phenomena were observed in typical mossy fiber boutons. Despite these degrading events, no electron-dense degenerating terminals were found. These results on naturally occurring nondegenerative synaptic degradation are discussed with current concepts of synaptic turnover and remodelling in the developing, adult and aging brain.

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