ROLE OF NEURONS IN THE LATERAL HABENULA FOR THE EXPRESSION OF MATERNAL-BEHAVIOR

The majority of experimental studies of maternal behavior have focused on rodents, with laboratory rats receiving the most attention. The pr incipal components of maternal behavior in the rat are retrieving, nes t building, and nursing or crouching behavior. When rat pups become di splaced from the nest area, a maternal female retrieves them to the ne st by carrying them in her mouth. A maternal rat also constructs a nes t with high walls to keep her pups warm and together in one place wher e they can be protected from predators. Retrieving and nest building a re considered oromotor components of maternal behavior because the fem ale picks up and carries pups or nest material in her mouth. During nu rsing behavior, a nonoromotor component of maternal behavior, the fema le exposes her ventrum to the pups by crouching over them in the nest area. The regulation of maternal behavior in the rat occurs in two pha ses.(1,2) The natural onset of maternal behavior occurs at parturition and is controlled by several pregnancy-related hormones (estrogen, pr ogesterone, prolactin, and possibly oxytocin). However, if a pregnant female is given rat pups supplied by another female just prior to part urition, she will display all components of maternal behavior. Thus, t he hormonal onset of maternal behavior occurs immediately prepartum an d is not dependent on hormonal or experiential factors associated with parturition. The maintenance phase of maternal behavior occurs during the postpartum period and is controlled primarily by nonhormonal fact ors (i.e., the multisensory stimuli provided by pups). As the postpart um period advances, the importance of hormones for maternal behavior w anes, while the stimuli provided by pups become important in controlli ng the duration of maternal behavior. Several investigators have demon strated that a brain region called the medial preoptic area is essenti al for the hormonal onset and nonhormonal maintenance of maternal beha vior in rodents.(2) Lesions placed in the medial preoptic area severel y disrupt the expression of all components of maternal behavior, where as minute amounts of estrogen implanted in the medial preoptic area, a n area rich in neurons containing estrogen receptors, induce maternal behavior. Moreover, the onset of maternal behavior can be disrupted by placing antiestrogens in the medial preoptic area. (Antiestrogens pre vent estrogen from acting on neurons containing estrogen receptors.) T his review focuses on the role of the lateral habenula for the express ion of maternal behavior. The medial and lateral habenula are two anat omically distinct subdivisions that together make up the brain's haben ular complex.(3) Several forebrain and midbrain structures that are co nnected with the medial preoptic area and are important for maternal b ehavior are also connected with the lateral habenula. The medial haben ula, in contrast, is not connected with the majority of brain regions that are known to mediate maternal behavior. Although the lateral habe nula has seldom figured prominently in the discussion of the neural ba sis of hormone-dependent motivated behavior, we began investigating th e importance of this region for the onset of maternal behavior for two reasons. First, as noted, the lateral habenula is connected with seve ral brain regions controlling maternal behavior. In addition, because the lateral habenula is important for other estrogen-dependent behavio rs, such as sexual behavior in the female rat,(3,4) it may also mediat e the estrogen-dependent onset of maternal behavior. Although very few neurons in the lateral habenula contain estrogen receptors, estrogen signals critical for the onset of maternal behavior could gain access to the lateral habenula from the medial preoptic area via several dire ct and indirect neural routes. For example, neurons containing estroge n receptors project from the medial preoptic area to the ventral tegme ntal area of the midbrain, which in turn projects to the lateral haben ula.(5)