Prepartum changes in maternal responsiveness and nest defense in Rattus norvegicus

Changes in maternal responsiveness during late pregnancy were traced by exposing females to foster pups (15-30-min tests) under conditions favoring the rapid initiation of maternal behavior. Groups were tested when nonpregnant or on Days 17, 20, 21, or 22 of pregnancy (Day 22 = parturition). Nulliparous females were compared with primiparous and with "experienced breeders." Nest defense was observed by introducing unfamiliar males (2-min tests) on Day 22. Results focused attention on three periods: (a) Days 17-20, when maternal responsiveness was lower than in the nonpregnant condition, (b) Day 21, when maternal responsiveness returned to or rose above nonpregnant levels, and (c) on Day 22, the 3.5 hr prior to delivery, during which 90% of females almost immediately retrieved, gathered, and tended foster pups and during which 92% attacked the unfamiliar intruders. (Attacks were rare earlier.) Maternally experienced females were more responsive to pups than nulliparous females when nonpregnant and throughout late pregnancy, but both groups were equally likely to show prepartum aggression.     

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.     

Enhanced feminine sexual behavior and infertility in female rats prenatally treated with an antiestrogen

An attempt to elucidate the possible role of prenatal estrogen on the development of feminine sexual behavior and reproductive function was made by treating females with the antiestrogen CI628 prenatally on days 13-19. Control females were prenatally treated with saline or remained untreated. The animals were delivered by caesarian section on day 22 of pregnancy and placed with foster mothers whose newborn pups had been previously removed. Intact peripubertal females in each treatment group were observed for several reproductive measures, including the capacity to become pregnant. Other females were ovariectomized in adulthood and treated with estradiol benzoate (EB) (1, 1.5, 2 or 4 micro g/rat) and 0.5 mg progesterone and tested for receptivity, proceptivity and sexual partner preference. Two weeks after the completion of these tests, the females were injected daily for 7 days with 0.25 mg testosterone and tested for sexual partner preference and mounting behavior. The results obtained showed accelerated vaginal opening, and infertility in the antiestrogen-treated intact females and enhanced receptivity and proceptivity in response to 1 micro g EB in the antiestrogen ovariectomized females. Sexual partner preference and mounting behavior did not differ between groups. These results suggest an involvement of prenatal estrogen on the development of female reproductive function, but not on behavioral differentiation.     

Differential Effects of Short- and Long-Term Early Maternal Separation on Subsequent Maternal Behavior in Rats

Female Sprague-Dawley pups were separated from mothers every other day for 8 hr (long-term separation/LTS), 4 hr (short-term separation/STS), or 0 hr (no separation/NS) from postnatal day 2–20. In adulthood, they were mated and tested for maternal behaviors during two lactations. It was expected that females separated from mothers as pups would show deficits in maternal behavior as adults. Contrary to expectations, LTS showed better nest building and grouped young faster during both lactations. LTS were first to display aggression and displayed more aggression during the second lactation. Notably, while some measures decreased from first to second lactation in NS and STS, LTS maintained levels of maternal care. These results suggest that extended periods of maternal separation may exaggerate some aspects of maternal behavior.     

Effects of transections to the vomeronasal nerves or to the main olfactory bulbs on the initiation and long-term retention of maternal behavior in primiparous rats.

While the onset of maternal behavior at parturition is mediated by hormones, the maintenance of maternal behavior during the first few postpartum weeks depends on experiences acquired while the dam interacts with pups (Rosenblatt, 1990). In fact, if female rats are permitted as little as 2 h or maternal experience within 36 h after Cesarean delivery, they exhibit heightened maternal behavior during maternal induction tests 10 days later; in contrast, dams separated from young at the time of Cesarean delivery and not permitted a maternal experience fail to respond maternally in tests 10 days later (Orpen & Fleming, 1987). In this study we investigated the role of chemosensory input through the vomeronasal and main olfactory systems in this maternal experience effect. Six groups of primiparous females were tested for maternal behavior to foster pups presented 9-10 days after Cesarean delivery: three groups were permitted to interact with pups for a 2-h period 36 h after Cesarean delivery; and three groups were separated from pups until testing and were given no maternal experience. Within each experience condition, one group sustained bilateral section of the vomeronasal nerves, one sustained bilateral coronal cuts through the midsection of the main olfactory bulbs, and one group sustained small medial olfactory bulb cuts. The results showed that animals sustaining vomeronasal or olfactory transections, regardless of experience condition, exhibited significantly reduced latencies to maternal behavior in maternal induction tests. However, these chemosensory disruptions did not prevent an additional facilitation of maternal behavior produced by a prior maternal experience.     

Evidence that a factor besides progesterone, prolactin, or plasma-estradiol-binding protein inhibits estrogen-induced sexual receptivity in pregnant rats.

Daily administration of estradiol benzoate stimulated significantly less lordotic behavior in rats during the second half of pregnancy than in ovariectomized females that received subcutaneous progesterone implants, pituitary grafts that raised plasma prolactin, or both treatments combined. Following an initial facilitation of receptivity, females with progesterone implants showed only moderate reductions in lordosis quotients over 3 test days. The capacity of plasma from pregnant rats to bind estradiol was found to increase significantly during the second half of pregnancy. However, daily administration to pregnant rats of a synthetic estrogen, R 2858, which is not bound by plasma protein, was no more effective than estradiol benzoate in stimulating receptive behavior. Administration of estradiol benzoate also stimulated significantly lower levels of sexual behavior in pregnant females than in females in which pseudopregnancy had been prolonged by previous hysterectomy or induction of uterine decidualization. These findings suggest that some endocrine factor other than progesterone, prolactin, or estradiol-binding protein is primarily responsible for the potent suppression of behavioral responsiveness to estrogen which occurs in pregnant rats. It is suggested that 5 alpha-reduced androgens may cause these behavioral effects.     

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.     

Nonselective maternal bonding but pup recognition in the subterranean rodent Ctenomys pearsoni

This study characterizes the maternal behavior in the subterranean rodent Ctenomys pearsoni and determines whether lactating females develop a selective bonding to their own pups in addition to maternal responsiveness. Mother-litter interactions were observed daily for 2 months; during the 1st postpartum week, selectivity and preference tests for own or alien pups were performed. Lactating females exhibited all patterns of maternal behavior observed in other rodent species and equally responded with care-taking behaviors to their own and alien pups, although they were able to discriminate between them, showing preference for their own pups. Results are discussed, taking into account the possible role of this behavior in shaping different aspects of life underground in ctenomyid species.     

Olfactory basis for the delayed onset of maternal behavior in virgin female rats: experimential effects.

A previous study showed that intranasal zinc sulfate (ZnSO4) treatment shortens the latencies for the onset of maternal behavior in nonpregnant rats. The aim of this study was to see whether after recovery from the effects of ZnSO4 treatment, the latencies for maternal behavior increased. In Experiment 1 nonpregnant females were intranasally infused with ZnSO4 or air or were left untreated and exposed to pups starting 48 hr later. Olfactory discrimination tests using chocolate bits were done simultaneously. The ZnSO4 treatment resulted in short latency maternal behavior (1.1 days) compared with latencies of control females (3.8 days), but neither group showed any loss of olfactory discrimination. Three weeks later- ZnSO4-treated females showed increased latencies for all but retrieving, while control groups showed decreased latencies for all maternal behaviors. In Experiment 2, intranasal ZnSO4- and air-treated females were given olfactory discrimination tests under food deprivation, using chocolate bits and guinea pigs pellets. Choice of guinea pig pellets was more severely affected than choice of chocolate bits, but recovery of the discriminations was complete in 4-5 days. The effects of ZnSO4 on maternal behavior and on olfactory discrimination in nonpregnant females were discussed.     

Prepartum and postpartum open-field behavior and maternal responsiveness in mice bidirectionally selected for open-field thigmotaxis

The authors examined pre- and postpartum open-field (OF) behavior and maternal responsiveness in mice that they bidirectionally selected for OF thigmotaxis. The authors tested 40 female mice under 3 conditions: prepartum OF, postpartum OF, and a pup retrieval test. In both OF conditions, the high OF thigmotaxis (HOFT) mice were more thigmotactic but explored and reared less than the low OF thigmotaxis (LOFT) mice, indicating that the HOFT mice were more emotional. In the postpartum condition, the HOFT mothers also defecated more and ambulated less than the LOFT mothers. The increase in grooming after parturition was more conspicuous among the LOFT mothers than among the HOFT mothers. The LOFT mothers were also more attracted to their pups in the OF, but the retrieval test did not show any substantial line differences. The results suggested that the line difference in emotionality was more pronounced during lactation than during pregnancy, although parturition exerted no effect on thigmotaxis.     

Maternal responsiveness to infant Norway rat (Rattus norvegicus) ultrasonic vocalizations during the maternal behavior cycle and after steroid and experiential induction regimens

When removed from the nest and placed in a cool environment, Norway rat (Rattus norvegicus) pups emit ultrasonic vocalizations that can elicit maternal search behavior. The authors examined the behavior of pregnant dams, mothers, and virgin females during exposure to a pup that was either warm and silent or cool and vocalizing. Results indicate potentiated maternal reactions to a vocalizing pup: Mothers approached and maintained proximal orientation to a vocalizing pup far more than did virgin females. Elevated levels of proximal orientation appeared within hours of birth, increased during the 1st week postpartum, and declined by the time of weaning. Estrogen plus progesterone administration facilitated virgin females' proximal orientation toward vocalizing pups, whereas prolonged exposure to pups in the absence of hormones was without effect, suggesting that the ontogeny of the maternal response is regulated, at least in part, by maternal hormones.     

Medial preoptic area and onset of maternal behavior in the rat.

The present series of experiments examined whether the medial preoptic area (MPOA) is involved in the onset of maternal behavior in the rat. Previously, the MPOA had been shown to be important in the maintenance of maternal behavior in the lactating rat. The first experiment investigated whether estradiol benzoate (EB) acts on the MPOA to facilitate the onset of maternal behavior in the 16-day pregnant, hysterectomized, and ovariectomized female rat. Such rats when given EB implants in the MPOA had significantly shorter latencies for the onset of maternal behavior than had females implanted with cholesterol in the MPOA or with EB in the ventromedial hypothalamus, in mammillary bodies, or under the skin. A second experiment showed that estrogen-induced prolactin release was not involved in this facilitation. A third experiment indicated that MPOA lesions disrupt the onset of maternal behavior that is induced by pup stimulation in virgin females. It was concluded that the MPOA is involved not only in the maintenance of maternal behavior but in the hormonally mediated onset of maternal behavior and the onset of maternal behavior induced in virgin females by pup stimulation.     

Interfemale aggression in adult bank voles (Clethrionomys glareolus)

Agonistic interaction may play a large role in shaping the social structure and spatial distribution of rodents such as Clethrionomys glareolus. Aggressive and non-aggressive behaviors of adult bank vole females were investigated with a home cage test during 10 min sessions. The number of attacks was significantly higher in virgin females kept with intact adult males than in singly reared females or those exposed to male urine. Bulbectomy of the tested females completely inhibited the male stimulating effect. This indicates that males influence the behavior of females by activating their olfactory systems. Aggressive behavior in pregnant or lactating females, which is linked to maternal behavior, was also tested. Female bank voles between 11 and 17 days of pregnancy or lactating at 3–4 days or 9–10 days attacked their partners significantly more frequently than virgins did. Females that had direct contact with males, even if they were not fertilized, appeared to be more successful in same-sex competition. Aggr. Behav. 24:53–61, 1998. © 1998 Wiley-Liss, Inc.     

Maternal aggression toward infanticidal males of different social status in wild house mice (Mus musculus domesticus)

Maternal aggression was examined in wild female mice (Mus musculus domesticus) derived from animals trapped in Alberta, Canada. Lactating females were tested for their behavior toward intruder males during the time of postpartum estrus while housed in a two-cage apparatus containing a defensible nest area. Prior to being used as intruders, sexually naive males were screened for their behavior toward a newborn pup (83% exhibited infanticide). Only infanticidal males were then housed in pairs and allowed to establish a dominance hierarchy. Dominance status was further verified by a urine marking test. The dominant and subordinate infanticidal males were then placed into a lactating female's cage and observed for 1 hr. The test was terminated immediately when a male began to attack the pups. Lactating females attacked the males in both groups, but subordinate males received more intense attacks than dominant males. Dominant males elicited significantly more fear/defense behavior than subordinate intruders. All of the dominant males and only one submissive male attacked the pups. Females were thus successful in blocking infanticide only by infanticidal subordinate males. Since females do not persist in attacking males with high fighting ability, one function of maternal aggression could be to assess the fighting, and resource holding, potential of a future mate. © 1994 Wiley-Liss, Inc.     

Cycloheximide blocks the retention of maternal experience in postpartum rats

Two studies were done to determine the effects of cycloheximide (CYX), a protein synthesis inhibitor, on maternal experience effects in rats. In the first study eight groups received a 2-h maternal experience 36 h after cesarean (c)-section and two groups received no post c-section experience. Among the experienced groups, two received icv injections of CYX or saline (SAL) 30 min before the maternal experience, two received CYX or SAL 10 min after the experience, and two received the injections 24 h after the experience. One inexperienced group received CYX and the other received SAL 36 h after c-section. Tests for maternal behavior occurred 10 days after c-section. CYX was not able to block or disrupt the "acquisition" or expression of ongoing maternal behavior during the 2-h experience phase. However, CYX was able to block the long-term "retention" of a 2-h maternal experience if the drug was present during or immediately after the experience, prior to "consolidation." The second study investigated the effects of CYX administered immediately after the maternal experience on the expression and retention of maternal behavior 4 and 6 days after c-section, to determine whether the hormonally mediated short-onset latencies of the 4-day group would be blocked by CYX. Eight groups of animals were tested for maternal behavior. Four were tested 4 days after c-section and four were tested 6 days after c-section. Within each of these groups two were experienced and two inexperienced; within each experience condition one group received CYX and one received SAL. Day 4 groups exhibited shorter onset latencies than Day 6 groups. There was also a CYX-SAL difference in maternal onset latencies among experienced Day 6 groups but not among Day 4 groups. These data indicate that the blocking effects of CYX can be seen only when hormonal priming of maternal behavior is no longer in evidence.     

Ingestive behavior in rat pups is modified by maternal sodium depletion

Developmental programming by maternal stress during pregnancy is found to influence behavioral development in the offspring. The main objective of this study was to investigate the effect of maternal sodium depletion in rats during pregnancy on the development of thirst mechanisms in the offspring. Pregnant rats underwent 3 episodes of saline depletion, induced by injecting sc 10 mg of Furosemide in saline (0.5 ml). The treatment, given on the 14th, 17th and 20th days post-conception, is thought to induce acute sodium depletion on dams. The offspring were tested for their drinking responses to Isoproterenol (500 μg/kg sc). In accordance to the known sequence of ontogenic development of drinking mechanisms, all groups of pups drunk after being stimulated with Isoproterenol at 6 days of age. The offspring from Furosemide-treated dams drank significantly less than the control group after Isoproterenol (p<0.001). Nevertheless, basal intake (water drunk after vehicle-saline only) was also significantly lower in these pups (p<0.001). In conclusion, offspring exposed to saline depletion in utero, modify their thirst responses at 6 day of age. This confirms that in utero conditions determine thirst responses in the offspring and they could provide adaptive advantages.     

Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster)

Pair-bonded prairie voles (Microtus ochrogaster) are biparental after the birth of pups. However, whereas most adult virgin males are parental, most virgin females are not. In 6 experiments, influences on the parental behavior of virgin female prairie voles were examined. It was found that (a) young virgin females were more maternal than older females, (b) the postweaning sex ratio of cage-mates did not affect females' responses to pups, (c) females raised to adulthood with their parents and younger siblings present were highly parental, (d) 48-hr exposure to pups beginning at weaning increased some aspects of later maternal responding, (e) rearing to adulthood with the parents even in the absence of younger siblings also increased females' maternal responding, and (f) the increase was seen only if both parents were present. Continued parental presence promotes alloparental behavior, possibly important if daughters do not disperse from the natal nest.     

A testosterone-mediated trade-off between parental and sexual effort in male mongolian gerbils (Meriones unguiculatus)

Effects of testosterone (T) on parental behavior of male Mongolian gerbils (Meriones unguiculatus) were examined. After undergoing gonadectomy, castrated males were implanted with empty capsules or capsules containing T; sham-operated males were implanted with empty Silastic capsules. Subsequently, each male was paired with a pregnant female, and after delivery, families were observed 15 min/day for 20 days. Gonadectomized males without T spent more time in contact with, huddling over, and licking pups than did either sham-operated males or gonadectomized males with T. When given a choice between nest sites and displaced pups, females and males with low T preferred pups, whereas intact males and castrated males with T preferred nest sites. The findings are consistent with E. D. Ketterson and V. Nolan's (1994) hypothesis implicating T in mediating trade-offs between parental and sexual effort.     

Perioral anesthesia disrupts maternal behavior during early lactation in Long-Evans rats

The role of perioral somatosensory stimulation from pups in maternal behavior was investigated in lactating Long-Evans rats (Rattus norvegicus) during early lactation by local anesthesia of the mystacial pads with lidocaine, which blocks conduction in the infraorbital nerve. It was concluded that (1) acute perioral anesthesia markedly inhibited pup retrieval when the subjects had no formal pretreatment retrieval experience. Further, these dams displayed little tolerance to the lidocaine treatment when they were tested repeatedly. (2) The severity of the effects of perioral anesthesia on retrieval was dependent upon prior experience and the testing situation. Following pretreatment retrieval experience, and in a test cage with dark and light compartments which provided a strong incentive to retrieve, 80% of lidocaine-injected dams did retrieve. However, retrieval efficiency was impaired by perioral anesthesia, largely due to increased time in contact with pups prior to each retrieval and to increased carrying time. (3) Perioral anesthesia also inhibited pup licking, but not self-grooming, suggesting that the former, but not the latter, is largely under peripheral stimulus control and that deficits in maternal oral activities cannot be due to impairment of mouth opening and use. (4) The onset of nursing behavior was delayed until after the recovery of snout sensations and retrieval. This suggests that a maternal behavior not directly involving the mouth is nonetheless dependent upon the dam's receipt of perioral tactile input from pups.