Jay S. Rosenblatt

Nonhormonal Basis of Maternal Behavior in the Rat

Rats were tested for induction of maternal behavior by exposing them to young pups continously for 10 to 15 days. Nonpregnant intact, ovariecto-mized. and hypophysectomized females were studied, as well as intact and castrated males. Nearly all the animals exhibited the four main items of maternal behavior and there were only minor differences in the latencies for the onset of maternal behavior among the various groups. It is concluded that all rats have a basic level of maternal responsiveness which is independent of hormonal stimulation.

HORMONAL BASIS DURING PREGNANCY FOR THE ONSET OF MATERNAL BEHAVIOR IN THE RAT

This article reviews the current state of our knowledge about the hormonal basis of maternal behavior in the rat. Considered are the ovarian hormones estrogen and progesterone, the pituitary hormones beta-endorphin and prolactin, and the hormone oxytocin, secreted by several hypothalamic nuclei and associated brain regions. The hormones of pregnancy, estrogen and progesterone, prime the female to respond to a terminal rise in estrogen that stimulates a high level of maternal responsiveness even before parturition begins. Studies on the role of prolactin, using hypophysectomy, prolactin release blockers and anterior pituitary and prolactin replacement, indicate that prolactin is required for the ovarian hormones to be effective in stimulating maternal behavior. During the latter half of pregnancy, placental lactogen may displace prolactin in this role. Although prolactin serves as a chronic stimulus for maternal behavior, it also may act over a short period. Oxytocin stimulates maternal behavior in a specific strain of rat, but not in other strains, and only when administered introcerebroventricularly (ICV) in estrogen-primed females. The decline in the high brain levels of beta-endorphin around parturition has been proposed as a requirement for the onset of maternal behavior; morphine blocks the onset of maternal behavior and disrupts ongoing maternal behavior and maternal aggression in lactating females. However, blocking beta-endorphin action at parturition interferes with pup cleaning and eating of the placenta as well.

Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period.

This set of experiments investigated the appetitive or motivational processes underlying the performance of maternal behavior. The place preference paradigm was adapted to simultaneously investigate the reinforcing properties of cocaine and pups for maternal, lactating dams. These modifications allowed the authors to assess which stimulus, either a 10 mg/kg s.c. injection of cocaine or 3 pups, had the strongest reinforcing value. At Postpartum Days 10 and 16, the dams preferred the cocaine cue-associated chamber, whereas the dams tested at Postpartum Day 8 preferred the pup cue-associated chamber. Overall, the data revealed an interaction between the postpartum period at testing and the exhibited preference for cocaine or pups. Further testing will investigate the neural circuitry underlying the appetitive processes of each stimulus.

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.

Decline of maternal behavior in the virgin and lactating rat.

Sensitized virgins and postpartum lactating mothers, both exhibiting maternal behavior, were given donor litters that increased in age by 1 day, for 28 days, starting at the onset of maternal behavior. Each day females were tested for maternal behavior with pups 4-8 days old: Maternal care (i.e., nursing/crouching, retrieving, nest building and licking) and maternal withdrawal, rejection, and prevention of nursing were recorded. After the ninth day, females were also tested with the progressively older pups from 10 to 28 days of age with which they were living. Virgins and lactating mothers showed generally similar patterns of maternal care although some differences were found, and they declined in maternal behavior toward the older pups in a similar manner. Maternal behavior did not decline in tests with younger pups. The results are interpreted as supporting the hypothesis that the decline as well as the maintenance of maternal behavior postpartum is nonhormonally mediated.

Maternal behavior in New Zealand white rabbits: Quantification of somatic events, motor patterns, and steroid plasma levels

Several parameters associated with maternal behavior were quantified under laboratory conditions in New Zealand white rabbits. Digging behavior appeared earliest (8-6 days prepartum), its decline preceding the onset of straw carrying (3-1 days prepartum). Hair pulling consummated the construction of the maternal nest. Food intake significantly decreased on days 2 and 1 prepartum. On parturition day, all females spent 300-500 s with the litter while, for the rest of lactation, nursing bouts lasted 199 +/- 7 s. Milk yield increased linearly up to lactation day 19, declining thereafter. Pup weight increased linearly throughout lactation despite the decline in milk yield. Plasma estradiol (E) levels did not significantly vary across pregnancy: 60 +/- 2 pg/ml (days 10-25) and 75 +/- 6 pg/ml (day 30). The testosterone (T) levels at these times were: 200 +/- 10 and 308 +/- 0.03 pg/ml, respectively. Testosterone significantly declined from pregnancy day 30 to lactation day 1 (202 +/- 0.02 pg/ml). Progesterone (P) levels significantly declined from pregnancy day 20 (9 +/- 1 ng/ml) onwards. Progesterone levels were negligible across lactation. Thus, mother rabbits display a sequence of motor patterns and somatic events correlated with changes in plasma levels of T and P against a background of E.

Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats

Lactating rats were used in experiments to examine the role of the dopamine system in the regulation of ongoing maternal behavior. Administration of haloperidol disrupted retrieval behavior and nest building in a dose-dependent manner but not nursing behavior and pup licking. Feeding behavior including carrying of food pellets to the nest and general locomotor ability were not disrupted by haloperidol. Apomorphine effectively reversed the inhibition caused by dopaminergic blockade. These results indicate a role for dopamine in the motivational regulation of retrieval and nest building during the postpartum phase of maternal behavior.

Aspects of nonhormonal maternal behavior in the rat

Abstract A new cross-transfusion procedure using single chronically implanted heart catheters was developed to permit animals to move freely during transfusion. Support for the concept of a nonhormonal basis of maternal behavior was found in the inability of blood, cross-transfused from pup-induced maternal virgins and spontaneous retrieving females, to shorten latencies for retrieving in recipient virgins. Spontaneous retrieving was not affected by the hormonal changes of pregnancy. On the other hand, the rate of induction of maternal behavior (i.e., retrieving) was shown to depend upon the size of the cage in which virgins were confined with pups: latencies were directly proportionate to cage area and opportunity for contact with pups.