Postnatal development of nonpyramidal neurons in the rat hippocampus (areas CA1 and CA3): a combined Golgi/electron microscope study

Abstract

This study describes the morphological differentiation of nonpyramidal neurons in areas CA1 and CA3 of the rat hippocampus as seen after Golgi-impregnation. Representative neurons were gold-toned and processed for an electron microscopic study of identified cells. We analyzed the postnatal stages P0 (day of birth), P5, P10 and P20. The results can be summarized as follows: 1. On the day of birth nonpyramidal neurons display relatively large cell bodies with short, clumsy dendrites. Great variability of the shape of the cell body and of the orientation of dendrites was observed when compared with the more stereotyped pyramidal neurons. Electron microscopy of identified nonpyramidal neurons revealed small infoldings of the nuclear membrane and immature synapses on the short dendritic shafts of these cells. 2. Developing nonpyramidal neurons from P0 and P5 display growth cones, filopodia, preterminal growth buds, and irregular varicose swellings along the dendrites. 3. Further postnatal development of nonpyramidal neurons is mainly characterized by an increase in dendritic length, paralleled by a decrease in growth cones and preterminal growth buds. By means of the electron microscope an increase in the number of mature input synapses on the gold-toned dendritic shafts of identified nonpyramidal neurons was observed. 4. There is a significant developmental difference between nonpyramidal neurons in CA1 and CA3 that was most obvious on P5. Nonpyramidal neurons in CA3 appear more mature, displaying longer dendrites that sometimes traverse through several hippocampal layers. In contrast, the dendrites of nonpyramidal neurons in CA1 are still restricted to the layer of the parent cell body. The earlier differentiation of nonpyramidal neurons in CA3 may result from the earlier formation of neurons in CA3 than in CA1. Longer dendrites of nonpyramidal neurons in CA3, together with an earlier arrival of afferent fibers in this region, suggest that nonpyramidal neurons in CA3 are integrated into inhibitory hippocampal circuits earlier than their counterparts in CA1. 5. On P20, hippocampal nonpyramidal neurons showed all structural characteristics as observed in adult animals both at light and electron microscopic levels. It is concluded that the structural maturation of hippocampal nonpyramidal cells is completed by that postnatal age.