The present study provides a comprehensive light and electron microscopic analysis of the anatomical organization of the rat mamillary body. The cytoarchitecture and morphology of mamillary neurons were investigated with the aid of Nissl-stained and Golgi-impregnated sections cut in transverse, horizontal, and sagittal planes. The ultrastructural features of the mamillary nuclei were correlated with observations made on Golgi material. The mamillary body is comprised of a lateral and a medial nucleus, the latter being subdivided into five major subnuclei: pars lateralis, pars basalis, pars medialis, pars medianus, and pars posterior. The perikarya are medium-sized or small with the proportions of each differing among subnuclei. The largest perikarya are found in the lateral mamillary nucleus (cell area 257.0 microns2) and have 2-5 radially oriented aspiny dendrites that are often beaded. Small cells predominate in the pars lateralis (cell area 116.3 microns2) and pars basalis (cell area 118.3 microns2), whereas the pars medialis (cell area 196.7 microns2), pars medianus (cell area 136.5 microns2), and pars posterior (cell area 154.6 microns2) contain mainly medium-sized cells. The dendrites of most cells in the medial nucleus are radially oriented and exhibit a variety of spines including numerous short stubby spines, spines with thin necks that end in spherical swellings, and long thin spines. Neuronal somata are often closely apposed with no intervening glial processes and contain eccentrically located nuclei with one or more invaginations of the nuclear envelope. Two main classes of axon terminals were identified in the mamillary body. One type contains round vesicles and forms asymmetric synaptic junctions (RA) with dendrites and dendritic spines. RA terminals rarely contact neuronal somata and proximal dendrites in the MB. The second type contains pleomorphic vesicles and forms mainly symmetric synaptic junctions (PS) with neuronal somata as well as dendrites and spinous processes. Dense-cored vesicles were frequently seen in both types of terminals. Both types of terminals often synapse with two adjacent dendrites and are also found near or adjacent to each other on the same dendrite. A quantitative analysis indicated that the numbers of RA terminals in the medial nucleus almost equals the numbers of PS terminals, whereas the lateral mamillary nucleus contains considerably more PS (64%) than RA terminals (36%).