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      Estrogen, Progesterone, and Pregnancy Termination Alter Neural Activity in Brain Regions That Control Maternal Behavior in Rats

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          Estrogen stimulates maternal behavior in rats, but does so most potently when its administration is temporally coupled with the termination of pregnancy. In contrast, this effect of estrogen is blocked when subjects are administered a large dose of progesterone concurrent with estrogen. The current study was performed to examine the neural circuitry influenced by these treatments and pup presentation during the hormonally-mediated onset and inhibition of maternal behavior. In experiment I, estrogen induced c-Fos immunoreactivity (Fos-IR) in the medial preoptic area (MPOA) in virgin rats, but was much more effective when administered to pregnancy-terminated rats, suggesting that pregnancy termination increases MPOA’s susceptibility to the physiological effects of estrogen. In experiment II, administering progesterone concurrently with estrogen in pregnancy-terminated rats strongly inhibited estrogen-stimulated Fos-IR in the MPOA, indicating that the physiological effects of estrogen on the MPOA are blocked if high progesterone levels are maintained. In experiment III, pregnancy-terminated subjects were administered estrogen, progesterone, or both hormones and presented with pups for 2 h. Approximately half of the subjects administered estrogen alone showed maternal behavior, but subjects receiving the other treatments were not maternal. In the MPOA, ventral bed nucleus of the stria terminalis (BSTv), and dorsal and intermediate lateral septum (LSd,i), maternal subjects showed the highest levels of Fos-IR, whereas subjects treated with progesterone alone or progesterone in combination with estrogen showed low levels of Fos-IR. These experiments suggest that estrogen could promote maternal behavior by enhancing pup-stimulated activity in the MPOA, BSTv, and LSd,i, regions believed to constitute the neural circuit that promotes maternal behavior, whereas progesterone could inhibit maternal behavior by inhibiting neural activity in some of these regions.

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          Most cited references 10

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          Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat.

          Prolactin has a variety of important physiological effects on peripheral tissue and on the brain. The behavioral effects of prolactin include the induction of maternal behavior and increased food intake. Prolactin acts via its cognate receptors which have two forms, a short and a long form. The long form of the receptor is predominant in the preoptic area-hypothalamus and is positioned to support maternal behavior since this form is regulated across pregnancy and lactation (Nagano and Kelly [1994] J. Biol. Chem. 269:13337-13345; Sugiyama et al. [1994] J. Endocrinol. 141:325-333). By using in situ hybridization with [33P] labelled cRNA probe specific for the long form of the receptor mRNA(L-PRL mRNA) we have mapped, in brains from 2- and 21-day-old pregnant females, the neuroanatomical distribution of neurons expressing the long form of the receptor. Many neurons with high expression of L-PRL mRNA were located in the anteroventral periventricular nucleus, the medial preoptic area (MPO), specific subdivisions of the paraventricular and supraoptic nuclei, and in the arcuate and ventromedial nuclei. Labelled neurons were also found in limbic system structures such as the bed nucleus of stria terminalis (BST) and the medial nucleus of the amygdala, in a few thalamic nuclei, and in the central gray. All cells throughout the choroid plexus expressed high levels of L-PRL mRNA. The levels of L-PRL mRNA were higher in females on day 21 of pregnancy in the MPO and in the choroid plexus, than in females on day 2 of pregnancy; levels in the ventromedial nucleus of the hypothalamus (VMH) were unchanged across pregnancy. The neuroanatomical distribution of neurons expressing L-PRL mRNA may have special relevance for the mediation of maternal behavior, lactation, sexual behavior, and feeding.
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            Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat.

            Previous studies in rats have demonstrated that large lesions in the medial preoptic area (MPOA) disrupt all aspects of maternal behavior. In the present study, small bilateral electrolyte lesions in the MPOA of lactating females abolished nest building and retrieving components of maternal behavior while crouching and nursing were unaffected. Animals which failed to show retrieval and nest building behaviors tended to have a greater area of lesion within the more dorsal part of the MPOA. Although the dorsal MPOA may play a role in the maintenance of the active components of maternal behavior, i.e. nest building and retrieving, another critical factor in determining which components of maternal behavior are disrupted may be the size of the lesion. As one increases the area of damaged tissue there is also an accompanying increase in the components of maternal behavior which are disrupted. No correlation was found between damage to the Sexually Dimorphic Nucleus of the preoptic area and retrieving and nest building.
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              Hormonal induction of maternal behavior in the ovariectomized nulliparous rat.


                Author and article information

                S. Karger AG
                January 2002
                24 January 2002
                : 75
                : 1
                : 12-23
                Boston College, Psychology Department, Chestnut Hill, Mass., USA
                48217 Neuroendocrinology 2002;75:12–23
                © 2002 S. Karger AG, Basel

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                Page count
                Figures: 4, References: 50, Pages: 12
                Regulation of Reproductive Functions


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