A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat

Abstract

The regulation of the onset of maternal behavior in the rat is under hormonal control. This study reports a new endocrine model for the study of the hormonal regulation of maternal responsiveness. The model employs the administration of physiological amounts of the steroids estradiol (E2) and progesterone (P) via Silastic implants to inexperienced nulliparous rats and measurement of the effects of these implants on maternal behavior. In the first two experiments, the levels of E2 and P in the sera of pregnant and hormone-treated rats were measured by RIA. Using known physiological treatments of E2 given in combination with P, the effects of E2 and P on maternal behavior were measured. Treatment with a combination of E2 at all dosages plus P for 2 weeks before P removal and behavioral testing stimulated a fast onset of maternal behavior in ovariectomized nulliparous rats. Exposure for 2 weeks to small E2 implants (1 or 2 mm; approximately 20-30 pg/ml serum) did not affect maternal responsiveness, whereas large E2 implants (10 mm; approximately 110 pg/ml serum) stimulated maternal behavior. P treatment alone had no behavioral effect. Simultaneous removal of E2 plus P before exposure to foster young also resulted in a stimulation of behavioral responsiveness, indicating that the presence of elevated titers of circulating E2 is not a requirement for stimulation to occur. In addition to facilitating a rapid onset of behavior, the quality of the response in steroid-primed rats was similar to that measured in lactating rats in a T-maze test. In another experiment, when female rats were treated with P before E2 administration, maternal behavior was rapidly induced. Thus, P itself can sensitize the female to the behavioral effects of E2. Finally, the duration of steroid-exposure before testing was found to influence maternal behavior. Increased durations of E2 plus P exposure before testing were accompanied by decreased latencies to respond maternally to foster young. These data indicate that during pregnancy, E2 and P prime the female to respond to her young at birth. The intensity of the steroidal priming increases as pregnancy progresses, and this primed potential is subsequently unmasked by the decline in P and the maintenance of E2 secretion around parturition. These findings demonstrate that behavioral processes can be modified in the adult animal as a result of long term changes in endocrine state, i.e. pregnancy.