Harold I. Siegel

Progress in the Study of Maternal Behavior in the Rat: Hormonal, Nonhormonal, Sensory, and Developmental Aspects

Publisher Summary This chapter discusses the progress that has been made in the study of maternal behavior in the rat with special focus on the research that has been carried out at the Institute of Animal Behavior. It describes how maternal behavior arises from the hormonal conditions that exist during pregnancy, particularly around parturition when maternal behavior normally begins. The chapter demonstrates that the maternal behavior cycle is a developmental product of hormonal events during pregnancy, especially at its termination, and of behavioral stimulation received during interactions between the mother and her young. Investigation of females whose pregnancies were terminated prematurely by hysterectomy and/or ovariectomy has shown that the rise in estrogen, primarily, is responsible for the onset of maternal behavior under these conditions. To be effective this rise must occur free of the inhibiting influence of high levels of progesterone and that the decline in progesterone in addition to its permissive action with respect to estrogen may itself facilitate a short-term increase in maternal responsiveness. The chapter further deals with postpartum stimulus factors, which regulate maternal behavior and are involved in its maintenance and eventual decline.

Estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats

Abstract A single injection of 100 μg/kg estradiol benzoate (EB) either alone or in combination with 0.5 mg progesterone resulted in a significant reduction in the latency for the onset of maternal behavior in hysterectomized-ovariectomized virgin rats as compared to the latencies of groups which either remained intact or were hysterectomized, hysterectomized-ovariectomized, hysterectomized-ovariectomized and treated with 20 μg/kg EB, or ovariectomized-sham hysterectomized and injected with 100 μg/kg EB. In contrast to recent research, there was no shortening of the maternal latencies when ovariectomy or combined hysterectomy-ovariectomy was performed 8 weeks prior to testing while the administration of EB 8 weeks postoperatively was still effective in stimulating short-latency maternal care in hysterectomized-ovariectomized females and increased the percentage of ovariectomized sham hysterectomized animals responding maternally. It was concluded that estrogen is capable of inducing, not suppressing, maternal behavior in virgin rats and that the uterus may play an important but as yet undetermined role.

Hormonal basis of hysterectomy-induced maternal behavior during pregnancy in the rat ☆ ☆☆

Abstract Hysterectomy during the last half of pregnancy (i.e., Day 10–19) induces a rapid onset of maternal behavior; ovariectomy in addition to hysterectomy, prevents this effect. Estradiol and progesterone were tested for their ability to restore short-latency maternal behavior in hysterectomized-ovariectomized (HO) females operated on the 10th, 13th, 16th and 19th days of pregnancy. A single injection of either 20 μg/kg or 100 μg/kg estradiol benzoate (EB) immediately following HO either alone or followed by 0.5 mg progesterone (P) 44 hr later restored short-latency maternal behavior similar to that observed following hysterectomy only. The lower dose of EB was found to be equally effective at all stages of pregnancy and P was unnecessary to induce maternal behavior. The effectiveness of EB in inducing maternal behavior was discussed in relation to the hormonal changes which follow hysterectomy during pregnancy and to those which are associated with the normal onset of maternal behavior around parturition.

Dietary self-selection by pregnant and lactating rats ☆

Abstract Protein-carbohydrate choice was studied in female rats through the course of the estrus cycle and during pregnancy and lactation. Both selecting and control diet fed animals grew at the same rates. Food intake was reduced during the estrus phase, but there were no changes in the dietary selection pattern. During both pregnancy and lactation protein intake was increased while carbohydrate intake was maintained at a level equal to nonimpregnated controls. These data were interpreted as supporting other studies showing that dietary self-selection follows the varying nutritional requirements of the organism.

Maternal aggression in rats: Changes over pregnancy and lactation in a sprague‐dawley strain

Maternal aggression in a Sprague-Dawley strain of laboratory rat (Charles River CD) was explored from Day 1 after mating on Day 0 through Day 24 of lactation (L0-L24). Aggression toward unfamiliar male “intruders” during 10-min tests was low among nonpregnant, nonlactating females and during the first 10 days of gestation. Frequency of attack on intruders increased moderately but significantly by Gestation Day 16 (G16; Experiment 1) or G21 (Experiment 2), a prepartum phenomenon not previously reported in laboratory rats. Levels of aggression were highest, however, during the first 9 days of lactation, when attacks averaged more than 6 per 10-min session. Attacks declined sharply in frequency after L14 and by L24 did not exceed levels observed among nonpregnant females. Experiment 3 examined the importance of the test site (home cage with nest and pups, if any, vs unfamiliar cage without nest or pups) to agonistic behavior associated with pregnancy and lactation. Late pregnant females tested in a novel cage were not aggressive; however, females tested shortly after delivering their pups were highly aggressive, averaging over four attacks per 5-min session. In novel cage tests frequency of attack remained high through L4 but declined significantly by L7. These data are consistent with the hypothesis that maternal aggression at its onset is primarily under hormonal control, but becomes increasingly dependent upon external factors, presumably pup stimulation, during the postpartum period.

Progesterone inhibition of estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats.

Abstract Hysterectomized-ovariectomized virgin rats were tested for maternal behavior following treatment with 100 μg/kg EB immediately at surgery and either oil, 0.5 or 5.0 mg progesterone either 0, 24 or 44 hr following surgery. Stimulus pups were presented 48 hr postoperatively which is counted as Day 0 of testing. EB + oil-treated females displayed short-latency maternal behavior beginning on Day 0. The injection of 5.0 mg progesterone at 0, 24, or 44 hr significantly inhibited the onset of maternal care while the effect of the lower dose of progesterone depended upon the timing of its administration in relation to that of EB. At a dose of 0.5 mg, progesterone given 24 hr following EB, inhibited the appearance of maternal behavior but had no effect given at 44 hr, and resulted in only a partial delay when given at the same time as the EB. Possible mechanisms by which progesterone interfered with the display of maternal behavior were discussed.

Uptake of [6,7-3H]Estradiol-17β in ovariectomized rats, guinea pigs, and hamsters: Correlation with species differences in behavioral responsiveness to estradiol

The amount of estradiol benzoate with progesterone required to induce lordosis in ovariectomized hamsters was determined to compare the responsiveness of hamsters to estradiol benzoate with that of rats and guinea pigs. In addition, the uptake and metabolism of tritiated estradiol in ovariectomized rats, guinea pigs, and hamsters was examined in an attempt to correlate species differences in behavioral sensitivity to estradiol with possible differences in neural affinity for the steroid. A dose of nearly 90 mg/kg was required to induce lordosis in 100% of the hamsters compared with the 2-5 mcg/kg which is effective in rats and guinea pigs. In all 3 species, highest uptake of estradiol was in the uterus and anterior pituitary gland. In the rat and guinea pig brains, the hypothalamus took up more estradiol than either the cortex or midbrain. In the hamster, there were no consistent differences in brain uptake. The affinity of the uterus, anterior pituitary, and hypothalamus of rats and guinea pigs for estradiol was greater than that of hamsters. In all 3 species, estrone was the principal metabolite of estradiol found in the tissues. The authors suggest that the higher the endogenous levels of a steroid, the less sensitive the animal is to that steroid.

Effects of pregnancy hormones on maternal responsiveness, responsiveness to estrogen stimulation of maternal behavior, and the lordosis response to estrogen stimulation

The aim of the study was to determine whether there is an increase in responsiveness to estrogen stimulation of maternal behavior and lordosis responsiveness during pregnancy. Using separate groups of pregnancy-terminated females, we measured the initial maternal responsiveness of hysterectomized-ovariectomized (HO) females and their responsiveness to estrogen stimulation. Maternal behavior latencies were studied in females HO on the 8th, 10th, 13th, 16th, or 19th day of pregnancy (8HO-19HO) and in nonpregnant HO (NPHO) females. Groups were injected sc with estradiol benzoate (EB) in doses ranging from 0 to 200 microgram(s)/kg and tested for maternal behavior (retrieving, crouching, and licking pups). In addition, we investigated whether there is an increase during pregnancy (following HO) in lordosis responsiveness to estrogen stimulation. Lordosis behavior was studied in pregnant HO females (days 8, 16, and 22) and NPHO females given 0 to 200 microgram(s)/kg EB. There was an increase in maternal responsiveness in oil-treated HO females starting around midpregnancy. From early pregnancy on there was also an increase in maternal responsiveness to 20 microgram(s)/kg EB. In late pregnant females (16HO) there was a further increase with 50 microgram(s)/kg EB. There was no increase in lordosis responsiveness to EB stimulation during pregnancy; pregnant and nonpregnant HO females had the same EB threshold for stimulating lordosis behavior. The results of both studies were related to increases during the latter half of pregnancy in nuclear estrogen receptor concentrations in the MPOA, an area that mediates estrogen stimulation of maternal behavior, and the absence of such increases during pregnancy in the VMH, an area that mediates estrogen stimulation of lordosis behavior.

Tail-pinch facilitates onset of maternal behavior in rats

Abstract Previous reports indicated that non-maternal female rats display a component of maternal behavior, namely, ano-genital licking of pups during, but not after a mild tail-pinch. The present study extends these findings and demonstrates that intermittent applications of brief tail-pinches accelerate in a dose-dependent pattern, the onset of all components of pup-stimulated maternal behavior in virgins. This suggests that the behavioral effects of tail-pinch stimulation outlast the pinch period and are cumulative.

Factors Governing the Onset and Maintenance of Maternal Behavior among Nonprimate Mammals

This chapter will review what is known about the factors which regulate the onset and maintenance of maternal behavior among nonprimate mammals. Maternal behavior is an outgrowth of the endocrinological processes which regulate pregnancy and parturition; therefore, in order to understand the factors which govern its onset, it is necessary to study the endocrine control of pregnancy in each species. In addition, many of the procedures used to investigate the onset of maternal behavior (e.g., hormone administration, hysterectomy, caesarean-section delivery, prostaglandin administration, ovariectomy, etc.) alter the normal course of pregnancy in specified ways that can only be understood with reference to the normal endocrine control of pregnancy.