Central Lactogenic Regulation of Maternal Behavior in Rats: Steroid Dependence, Hormone Specificity, and Behavioral Potencies of Rat Prolactin and Rat Placental Lactogen I*

Abstract

Adult virgin female rats display maternal behavior when continuously exposed to foster young for 5-6 days. Central infusions of PRL or placental lactogens (PLs) together with systemic treatment of progesterone (P) and estradiol (E2) stimulate maternal behavior in 1-2 days. In the present set of studies, it was asked whether the actions of lactogenic hormones are dependent upon both E2 and P and specific to lactogenic molecules. Moreover, we wanted to know whether central infusions of rat (r) PRL and PLs were equally effective in inducing maternal behavior. In the first study, adult virgin rats were ovariectomized (ovx) and stereotaxically fitted with bilateral cannulas directed at the medial preoptic area (MPOA). Rats were then assigned to one of four groups: P plus E2, blank (B) plus E2, P plus B, and B plus B. P-filled or B capsules were implanted sc on treatment day 1 and removed on day 11, whereas E2 or B capsules were implanted on day 11. All groups were infused with rPRL (40 ng/side) five times from days 11-13 and injected with bromocriptine (CB-154) sc (days 11-17) to suppress endogenous PRL release. Behavioral testing was conducted daily from days 12-17. It was found that exposure to both P and E2 was necessary to induce a fast onset of maternal behavior in PRL-infused females; priming with P or E2 alone in PRL-treated rats failed to stimulate a fast onset of behavior relative to that in nonsteroid-treated controls. In the second experiment to determine the biochemical specificity of PRL's action, adult nulliparous rats were ovx, implanted with bilateral cannulas directed at the MPOA, treated with both P and E2, injected with CB-154, and infused centrally (five times) with 40 ng (per side) of bovine GH, ovine LH, or vehicle. Central infusions of either bovine GH or ovine LH failed to stimulate maternal behavior, suggesting that the stimulatory actions of PRL are related to its lactogenic properties. In the final study, rats were ovx, fitted with bilateral cannulas directed at the MPOA; treated with P, E2, and CB-154; and given a single set of bilateral infusions of rPL-I or rPRL (40 ng/side.infusion) on day 11, three sets of infusions of rPL-I or rPRL (days 11 and 12), or vehicle infusions. Rats given three infusions of rPL-I and rPRL responded faster than controls, although the effect was not as robust as that in animals given five infusions in the initial study. rPL-I and rPRL groups did not differ from one another. Together these studies indicate that 1) both P and E2 are required for lactogenic stimulation of maternal behavior; 2) the stimulatory actions of PRL and rPLs on maternal behavior are related to their lactogenic properties; 3) extended treatment of females with lactogenic hormones is more effective in stimulating the onset of maternal behavior; and 4) the neural potencies of rPRL and rPL-I are similar. These findings provide support for the idea that the induction of maternal behavior is stimulated by the central actions of lactogenic hormones.

Prolactin: A Pleiotropic Neuroendocrine Hormone

“…Interestingly, animals with a disrupted prolactin gene exhibit some maternal behaviour (133), presumably mediated through activation of prolactin receptors by placental lactogen. Consistent with what is known about the neuronal circuitry regulating maternal behaviour, it appears that the action of prolactin or placental lactogen to stimulate maternal behaviour is exerted in the medial preoptic nucleus (134).…”

Region‐Specific Expression and Hormonal Regulation of the First Exon Variants of Rat Prolactin Receptor mRNA in Rat Brain and Anterior Pituitary Gland

“…PRL secreted from the anterior pituitary gland acts on these neurones to stimulate dopamine release into the pituitary portal vessel, which in turn gives rise to a reduction in pituitary PRL secretion. The medial preoptic area is believed to be the region responsible for PRL-induced maternal behaviour (47). The present results suggest that a promoter for E1-3 (PIII promoter) is commonly utilised in the different nuclei expressing PRL-R in this area.…”

Reproductive Experience may Positively Adjust the Trajectory of Senescence

“…Other substances, e.g., prolactin, placental lactogens, oxytocin, endogenous opioids, etc. also fluctuate temporally and are vital to both pregnancy and parturition, as well as to the onset of maternal behavior (see, e.g., Bridges et al 1996Bridges et al , 1997Kinsley 1994). …”