Morphogenesis, distribution of cholinergic enzyme acetylcholinesterase and synaptogenesis in the dentate gyrus of the rhesus monkey during the pre- and postnatal periods of development were examined using histological, histochemical and ultrastructural methods. The pattern of neuronal differentiation in the dentate gyrus demonstrated distinct superficial-to-deep and lateral-to-medial gradients. The histochemical reaction for acetylcholinesterase was present on gestation day 120 as minimal staining in the supragranular band and in the inner one-third of the dentate molecular layer. At term, the laminar distribution of the enzyme assumed mature pattern although considerable enhancement in staining intensity was achieved postnatally. At term and at 9 months of postnatal age, the most pronounced enzyme activity was found in the supragranular band and in the inner one-third of the molecular layer. Synaptogenesis in the dentate molecular layer was characterized by the early formation of axo-dendritic contacts on dendritic trunks and branches followed by the appearance of synapses on simple and complex spines. Spines were detected infrequently on gestation day 132. On day 148, they ranged in morphology from short stubby protrusions to pedunculated, triangular processes. The majority of the spines exhibited flat postsynaptic surfaces. Complex, synapse-bearing U- and W-shaped spines were observed rarely at this age but appeared more frequently at term and at 15 months of postnatal age. However, at all ages, including 15 months postnatally, synapses on flat-surfaced simple spines predominated. Most synapses were of the asymmetric variety.With certain exceptions, these features of development of the rhesus dentate gyrus resemble the reported patterns of postnatal ontogenesis of this structure in the rat. However, the ingrowth of cholinergic afferents and the major modifications in synapse structure occur prenatally in the rhesus monkey during the second half of the gestation period. This temporal difference between the two species should receive consideration in the planning of neuroplasticity experiments designed to explore lesion-induced adaptations in afferent growth and synaptogenesis in the rhesus dentate gyrus.
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