Studies on the evolution of the mammalian brain suggest that changes in subcortical structures include the division of the once continuous bed nucleus of the stria terminalis (BST) and medial amygdaloid nucleus (MA). Within each of these two areas is a group of vasopressin (AVP) cells, which together form the sexually dimorphic AVP system. Studies carried out for this thesis answered questions on the development and morphology of this system, with special reference to the evolutionary relationship between its two AVP cell groups. The first study tested whether, when placed in the same environment, developing AVP cells of the BST and MA can innervate similar targets. AVP cells in BST or MA fetal grafts showed similar fiber outgrowth into the lateral septum of adult AVP-deficient Brattleboro rats, which is inconsistent with the paucity of AVP projections from the MA to the lateral septum of non-deficient rats. This inconsistency suggests that developing AVP cells of the BST and MA can respond to similar environmental cues. The second study tested whether the AVP cells of the BST and MA have similar birthdates. Combining AVP and bromo-5-deoxy-2-uridine (BrdU) immunocytochemistry suggests that most AVP cells within the BST and MA are born around embryonic days (E) 12-E13, which is surprising, since this and previous studies suggest that most cells within the same divisions of the BST and MA are born around E14-16. No differences were found between birthdates of AVP cells in the BST and MA. However, there were differences between males and females. Females had proportionally more AVP cells colocalized with BrdU on E13. The third study tested whether projections of AVP cells in the BST and MA are similar. Anterograde tracing suggests that AVP cells of the BST and MA contribute in different proportions to the innervation of forebrain areas that contain sexually dimorphic AVP fibers. Retrograde tracing combined with AVP immunocytochemistry suggests that more AVP cells in the BST project to the lateral septum than AVP cells in the MA. These studies raise questions about the structural and functional development of the mammalian brain. Using the sexually dimorphic AVP system as an example for other systems, some of these questions are discussed in the final chapter.