Development of principal pyramidal and granule cells and nonprincipal GABAergic neurons of the primate hippocampus

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Granule cells, hilar mossy cells, and CA3 pyramidal cells of monkeys are in an advanced stage of development at birth (Seress and Ribak, 1995a,b). Most granule cells have a complete dendritic arbor, although both spine density and the number of synapses in the molecular layer increase after birth (Seress, Baumgartner, and Ribak, 1995). Mossy cells and CA3 pyramidal cells display thorny excrescences, and terminals of mossy fibers (axons of granule cells) establish multiple synapses with those excrescences (Seress and Ribak, 1995a,b). These features indicate that in monkeys developmental events are mainly prenatal, but the chronological sequence of synaptic development is similar to what occurs in the rat. At present we have no data about the development of CA1 pyramidal cells in monkeys. Our preliminary data indicate a change in spine density and myelin formation up to the postnatal seventh month.

In conclusion, the monkey hippocampal formation displays a fast and dynamic development that terminates several months after birth. In harmony with the advanced stage of development of principal neurons, most GABAergic cells of the hippocampal formation mature very early in monkeys (Berger, Alvarez, and Goldman-Rakic, 1993; Berger, deGrissac, and Alvarez, 1999). This is in contrast to the development of non-principal cells in rats, where GABAergic neurons show a very immature appearance at birth (Seress and Ribak, 1990). Berger, Alvarez, and Goldman-Rakic (1993) assume that functional circuits are forming between the hippocampus and the entorhinal cortex of primates during the first half of gestation. Other data also suggest an early maturation of the human entorhinal cortex (Kostovic, Petanjek, and Judas, 1993; Ulfig, 1993). Light and electron microscopic data are sparse with respect to the developing human hippocampal formation. Nonetheless, the cell types and cytoarchitectonics of the adult hippocampus have been described in several classic reports (Koelliker, 1896; Lorente de No, 1934). Purpura (1975) has included the hippocampus in his description of the human cerebral cortex, but concentrated mainly on the early developmental stages. He observed that a variety of growth processes observed in hippocampal pyramidal neurons in the 20-29-week-old fetus are not prominendy displayed in granule cells. In 33-week-old premature infants, many granule cells display dendrites that appear to be mature, except for the total number of spines, whereas other granule cells display immature dendrites. The time period from 20 to 28 weeks of gestation is a phase of maximum dendritic growth for hippocampal pyramidal neurons (Purpura, 1975). Pyramidal neurons of the CA3 area display only a few, small spines (spicules) and filopodia on their dendrites in the 22-week-old fetus. In the 33-week-old fetus, the first thorn-like excrescences appear on the dendrites of pyramidal-type neurons of the hilus and on CA3 pyramidal cells, suggesting that the first connections between granule cells and their postsynaptic targets in the hilus and CA3 area are established by the 33rd gestational week.

In children born at term, the hilus of the dentate gyrus contains large multipolar cells displaying a few complex thorn-like excrescences and a few small, conventional spines (figure 4.8A; see color plate 7). These cells are probably young mossy cells that have already established a few synapses with mossy fiber terminals of granule cells (figure 4.9; see color plate 8). In agreement with the previous observations of Purpura (1975), we have demonstrated that well-developed granule cells frequently appear in the granule cell layer (figure 4.8C; see color plate 7). These granule cells have dendrites that display a large number of spines and an axon that gives rise to several collaterals in the hilus (figure 4.8C). In addition, several granule cells display varicose, stubby, short, and spineless dendrites that terminate in

Figure 4.8 Photomicrographs of Golgi-impregnated neurons in the human dentate gyrus. (A) Dendrites of the mossy cell in the newborn infant display the convendonal simple spines and a few small protrusions that can be thorny excrescences (arrows). (B) Dendrites of mossy cell of the 3-year-old child display large complex spines, the so-called thorny excrescences, that are characteristic for mossy cells of the adult brain (D). (C) Large numbers of granule cells display spiny dendrites (open arrows) and a richly arborizing axon (arrows point to the axon and its collaterals) in the dentate gyrus of the newborn child. Calibration bars = 40 Jim for B and 20 |im for A, C, and D.

Figure 4.8 Photomicrographs of Golgi-impregnated neurons in the human dentate gyrus. (A) Dendrites of the mossy cell in the newborn infant display the convendonal simple spines and a few small protrusions that can be thorny excrescences (arrows). (B) Dendrites of mossy cell of the 3-year-old child display large complex spines, the so-called thorny excrescences, that are characteristic for mossy cells of the adult brain (D). (C) Large numbers of granule cells display spiny dendrites (open arrows) and a richly arborizing axon (arrows point to the axon and its collaterals) in the dentate gyrus of the newborn child. Calibration bars = 40 Jim for B and 20 |im for A, C, and D.

growth cones (Seress, 1992). These latter granule cells are still growing and may be those that were formed in the perinatal period. Therefore, the diversity in granule cell development seen by Purpura (1975) in the 33-week-old fetus is still observable at birth. It should be noted that a few immature-looking granule cells are still seen in the 15-month-old child (Seress, 1992), suggesting that granule cells exhibit a prolonged period of cell proliferation. The first real thorn-like excrescences appear on mossy cells by the third postnatal month (Seress and Mrzljak, 1992). At seven months thorny excrescences are frequent on mossy cells, but their number and size continue to increase up to the third year, when the first adult-like mossy cells appear (figure 4.8B; see color plate 7). The complex spines or thorny excrescences of the adult human mossy cells (figure 4.8D; see color plate 7) are much larger than those in monkeys x^-r'i-;' *

Figure 4.9 Photomicrographs of Golgi-impregnated pyramidal cells in the cortex (A and B) and in Ammon's horn (C and D) of hippocampal formation in newborn (A and C) and adult (B and D) brain. Pyramidal cells in the newborn child display immature, beaded, spine-free short dendrites, whereas in the adult, pyramidal cells have large dendrites fully covered with spines. Calibration bar = 20 (im.

Figure 4.9 Photomicrographs of Golgi-impregnated pyramidal cells in the cortex (A and B) and in Ammon's horn (C and D) of hippocampal formation in newborn (A and C) and adult (B and D) brain. Pyramidal cells in the newborn child display immature, beaded, spine-free short dendrites, whereas in the adult, pyramidal cells have large dendrites fully covered with spines. Calibration bar = 20 (im.

or in rodents (Frotscher et al., 1991). In the 3-year-old child mossy cells still vary with respect to their dendritic spine density and the size of their thorny excrescences. Not until the fifth year do all impregnated mossy cells display similarly large thorny excrescences that are indistinguishable from those seen in adults (Seress and Mrzljak, 1992). The extended morphological development of granule, mossy, and pyramidal cells accords with the prolonged development of cytoskeletal proteins, since an adult pattern of neuronal cytoskeletal protein expression in the hippocampus appears around the second postnatal year (Arnold and Trojanowski, 1996b). There is a similarly extended development of thorny excrescences for CA3 pyramidal neurons, although it appears that CA3 pyramidal cells display more advanced thorns at birth than the mossy cells. Similarly, CA3 pyramidal cells of newborn monkeys appear to show more developed thorn-like excrescences than mossy cells (Seress and Ribak, 1995a,b). However, not only the mossy cells but also the pyramidal cells of the CA1 region of Ammon's horn are in an early stage of proliferation at birth. If the CA1 pyramidal cells of adults (figure 4.9D) are visually compared with the pyramidal cells of newborn infants (figure 4.9C), several differences are obvious. The pyramidal cells of newborn infants have few basal dendritic branches and poorly developed side branches of the apical dendrites. A similar pattern has been found in the neocortex, where the pyramidal cells of the newborn child display a few, varicose, short basal dendrites and a few poorly developed side-branches of the apical dendrite (figure 4.9A). There are only a few spines on the pyramidal dendrites of the newborn infant (figure 4.9A), whereas the equivalent pyramidal cell dendrites in the adult cortex are fully packed with spines (figure 4.9B). The postnatal human development of pyramidal cells in Ammon's horn and the neocortex has not been described in detail, but our observations suggest that the morphological development of the principal neurons of those brain areas lasts as long as that in the hilar region.

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