Postpartum aggression in mice: The influence of suckling stimulation

The influence of suckling stimulation upon postpartum aggression was studied by removing the nipples (thelectomy) of female mice at various times during pregnancy and lactation. Prepartum thelectomy, regardless of whether it was performed prior to mating or shortly before parturition, in combination with the fostering of young, prevented the exhibition of aggression. The aggressive behavior of females thelectomized following either 2 or 5 days of suckling experience was similar to that of normal lactating females. However, only 25% of animals thelectomized following 24 hr of suckling experience exhibited aggressive behavior. The results demonstrate that suckling stimulation is important for the initiation of postpartum aggression but is not essential in animals that have had at least 48 hr of suckling experience.     

Post partum aggression against intruding male conspecifics in sprague-dawley rats

Six independent groups of individually housed female rats of the Sprague-Dawley strain were given a 5-min aggression test on Day 0 (day of parturition), 3, 6, 9, 12, or 15 postpartum. Latency to attack male conspecifics differed reliably among groups, being shortest on Day 0. Significant group differences in frequency of aggressive acts were also found with a consistent reduction in all measures by the end of the second week of lactation. Although attack by females caused most male intruders to react defensively, 23% of intruders showed retaliatory attacks against females. The function of maternal aggression in protecting the pups from infanticide by unfamiliar males is discussed.     

Role of nipple stimulation in the suppression of estrous cyclicity during extended lactation in the rat

The role of nipple stimulation in the suppression of the estrous cycle during extended lactation was studied in rats subjected to either total, partial, or sham excision of the nipples. Each female cohabited with 4 pups, 4-14 days old, over a period of 70 days postpartum, during which vaginal smears were recorded daily. Initially, regardless of the presence of nipples, all rats exhibited a postpartum diestrus that lasted for 12-20 days. Intact females (bearing 6 pairs of nipples) continued to exhibit successive prolonged diestrous phases over 70 days of lactation. A comparable result was obtained with females bearing only the anterior pair of nipples, which, in a separate experiment, was found to be the most frequently suckled pair. However, females devoid of nipples resumed regular (4-day) estrous cycles between Days 12 and 27 postpartum, in spite of their continuous contact with pups. Thus, when lactation is prolonged beyond the normal time of weaning (Day 21 postpartum), stimulation of the nipples by sucking becomes indispensable for the continued arrest of the estrous cycle. The possible mechanisms underlying this phenomenon are discussed.     

Maternal aggression in hamsters: effects of stage of lactation, presence of pups, and repeated testing

This study investigated maternal aggression in hamsters and examined the effects of early versus late lactation, presence or absence of the litters during the tests, and prior aggressive encounters. There was a total of six experimental groups. Two groups were tested in the presence of their litters on both Days 5 and 15 of lactation; two groups were presented with intruders after a 6-hr interval of mother-litter separation on Days 5 and 15 of lactation. The last two experimental groups were tested on Day 15 only in the presence of their litters or after a 6-hr separation from their litters. Estrous-cycling animals were also tested twice (10 days apart) or once to control for periods of social isolation. Animals were tested in their home cages for 10 min with weight-matched estrous-cycling intruders. Sexually receptive females were not used as controls or intruders. Measures of aggression included fights, attacks, chases, and intruder retreats. Lactating animals initiated significantly higher levels of all measures of aggression than cycling controls. There were no differences in aggression between Days 5 and 15 of lactation or between the groups tested in the presence or absence of their litters. Prior testing on Day 5 had little effect on aggressive responses on Day 15. The results are discussed in terms of comparisons to other species and the factors responsible for high levels of aggression during lactation.     

Postpartum aggression in mice: Experiential and environmental factors

Six experiments were conducted to assess the influence of duration of lactation, the presence of young, and the stimulus characteristics of intruder animals upon postpartum aggression of mice. The first experiment showed that postpartum aggression toward conspecifics was highest between Day 3 and Day 8, declined between Day 9 and Day 14, and was present toward males but absent toward females between Day 15 and Day 21 of the lactation period. Experiment 2 showed that lactating mice rarely attacked conspecifics to which they had been previously exposed but would readily attack strangers. Experiment 3 and 4 demonstrated that lactating animals never attacked intruders when tested 5 hr after pup removal. However, placement of young behind a wire partition in the home-cage for 5 hr or replacement of the offspring for as little as 5 min following 5 hr of separation restored postpartum aggression. The fifth experiment showed that 1- and 10-day old intruders were seldom attacked while intense aggression was directed against 14- and 20-day old intruders. Finally, Experiment 6 demonstrated that 14-day old intruders whose hair was removed were rarely attacked.     

Hormonal factors influence the onset of maternal aggression in laboratory rats

This experiment addressed the hypothesis that aggressiveness toward conspecifics is stimulated by hormonal factors known to mediate the onset of maternal care. Subjects included both pregnant and virgin females. Sixteen-day pregnant rats were hysterectomized (H), hysterectomized-ovariectomized and injected with estrogen (HO-EB), or subjected to sham procedures. Nonpregnant females were HO-EB or sham operated. The females were sensitized by continuous exposure to pups and were judged to have initiated maternal care when all pups were retrieved and grouped, Aggressiveness was observed during 5-min intruder tests using unfamiliar males, administered (a) 10 min prior to the introduction of test pups, (b) following the first 3 hr of pup exposure, and (c) after females had initiated maternal care. The results revealed that treatments known to reduce sensitization latencies also increased aggressiveness even prior to exposure to pups. Aggressiveness was displayed before sensitization only in groups having elevated estrogen levels. After initiating maternal behavior, pregnant and pregnancy-terminated females increased further in aggressiveness whereas nonpregnant females did not. Pregnancy-terminated, HO-Oil females became aggressive (only) after initiating maternal behavior, indicating that factors other than estrogen also influence the onset of maternal aggression.     

The role of progesterone in pregnancy-induced aggression in mice

A series of six experiments was performed in order to explore the potential involvement of progesterone (P) in pregnancy-induced aggression (PIA) displayed by Rockland-Swiss mice toward adult male intruders. In Experiment 1, circulating levels of P and aggression were low on gestation Days 6 and 10 while both the behavior and the steroid reached peak levels by gestation Day 14. By gestation Day 18 (the day prior to parturition), serum P was at its lowest level yet aggressive behavior was still intense. Also, individual differences in the display of fighting behavior by pregnant females were not related to circulating P. Experiments 2 and 3 showed that supplemental P treatment to early pregnant female mice did not advance the onset of aggression. Experiment 4 showed that P treatment promoted the onset and elevated the incidence of aggression in virgin mice, but only in those females with intact ovaries. Experiment 5 showed that the aggressive behavior of P-stimulated virgin females was qualitatively and quantitatively different from that exhibited by pregnant mice in that the former exhibited fewer attacks and lunges than the latter. Finally, Experiment 6 showed that the removal of P from aggressive, P-stimulated virgins dramatically attenuated levels of the behavior. This contrasts sharply with the continued fighting behavior observed in late pregnant P-deficient mice. Thus, although P augments aggression in female mice it apparently is not a sufficient stimulus for producing pregnancy-like aggressive behavior.     

Further evidence for the role of nitric oxide in maternal aggression: effects of L-NAME on maternal aggression towards female intruders in Wistar rats

It has been shown that nitric oxide (NO) increases aggression in male mice, whereas it decreases aggression in lactating female mice and prairie voles. It is also known that aggression can be exhibited at different levels in rodent species, strain or subtypes. The aims of this study were to investigate the proportion of aggressiveness in Wistar rats, the effect of intraperitoneally administered nonspecific nitric oxide synthase (NOS) inhibitor L-NAME (NG-nitro L-arginine methyl ester) on maternal aggression towards female intruders, and whether these effects are due to NO production or not. Rats were given saline intraperitoneally on the postpartum Day 2 and aggression levels were recorded. The same rats were given 60 mg/kg L-NAME or D-NAME (NG-nitro D-arginine methyl ester) on the postpartum Day 3 and their effects on aggression levels were compared to saline. While L-NAME administration did not cause any differences in the total number of aggressive behavior, aggression duration and aggression intensity, it reduced the proportion of animals showing aggressive behavior. In addition, the latency of the first aggression was significantly increased by L-NAME. In the D-NAME group, however, no significant change was found. Our results have shown that L-NAME reduces maternal aggression towards female intruders in Wistar rats through inhibition of NO production. These results suggest that the role of NO in offensive and defensive maternal aggression shares neural mechanisms.     

Influence of Litter Gender Composition on Subsequent Maternal Behaviour and Maternal Aggression in Female House Mice

It has been suggested that the sex-dependent pattern of mother-pup interaction that occurs early in infancy can affect some aspects of the animal's behaviour repertoire in adulthood. The aim of this study was to investigate the effects of litter gender composition (LGC) on subsequent maternal behaviour and aggression in the female house mouse. Albino mouse litters were reduced at birth to six pups according to two conditions: FM (3 females and 3 males) and FF (all females). At weaning (day 21), all mice were rehoused in unisexual groups. At adulthood (70–90 days) the females were mated and litters culled at birth to 6 pups (3 females and 3 males). On days 2, 4, and 6 after delivery the females were tested for maternal behaviour (10 min) and retrieval of pups. On day 6, at the end of the recording of maternal behaviour, the females were also tested for maternal aggression towards a strange adult male conspecific (5-min exposure). In absence of differences in maternal behaviour scores, FM females showed shorter latencies for retrieval of the first pup on postnatal days 2 and 4. Maternal aggression was also significantly affected by the two conditions. FM females showed higher scores of both duration and frequency of aggressive grooming, defensive upright postures, fleeing and of the number of attacks. FF females spent more time self-grooming, crouching, and on nest. These results support the hypothesis that a series of factors, such as olfactory, tactile, and acoustic stimulation provided by the pups, the variation of maternal behaviour depending upon LGC, and the qualitative and/or quantitative variation in social interaction with the opposite sex in infancy, contribute to the broad interindividual plasticity to cope in different environmental situations.     

Effects of ergocornine and prolactin on aggression in the postpartum golden hamster

The effects on aggressive behavior of prolactin (PRL) and ergocornine hydrogen maleate, an inhibitor of PRL secretion, were investigated in the female golden hamster. Because high aggression and PRL levels are associated with lactation in hamsters, postpartum females were used as subjects. In the first experiment, three groups of ovariectomized and hysterectomized females were compared: normally lactating, ergocornine-treated, and ergocornine plus replacement PRL treated. Normally lactating mothers were typically aggressive towards males in an arena, whereas females given ergocornine were not. Females given both ergocornine and PRL showed an intermediate level of aggression. Although ergocornine suppressed aggression towards adult males, attacks on pups increased. A second experiment sought to determine if ergocornine would depress aggression when PRL involvement was unlikely. At least 30 days following pup removal, females from the first experiment were “trained” to attack home-cage intruders consistently. After ergocornine administration, home-cage attacks by these experienced females were not diminished. Since PRL levels were probably low in these animals, it was concluded that the effects of ergocornine on aggression were limited to instances in which PRL was involved, and that PRL probably can facilitate aggression.     

Prenatal stress and maternal behavior in intact virgin rats: response latencies are decreased in males and increased in females

The repeated findings that levels of various male-typical behaviors (e.g., copulatory behavior and intermale aggression) are reduced in prenatally stressed (P-S) males, coupled with reports of effects on female physiology and behavior, prompted us to examine the maternal behaviors of P-S animals toward young. Sprague-Dawley female rats were timed-mated (+ sperm = Day 1). From Gestation Days 15 to 22 experimental females were subjected to heat and restraint stress. Control females remained undisturbed throughout pregnancy. The offspring, as adults, were assessed for maternal behavior. P-S males exhibited a significantly shorter latency (in days) to show full maternal behavior (FMB) than Control males, median = 5.0 vs 8.0, respectively. P-S females, on the other hand, exhibited a significantly longer latency than Control females to show FMB (7.0 vs 3.0, respectively). as well as longer latencies to retrieve one, two, or three pups, to begin to crouch over pups, and to build nests in response to young. Sex differences were apparent between Control males and Control females (females were more responsive to young). In contrast, P-S males and Control females exhibited similar latencies to show components of FMB (3-5 days), as did P-S females and Control males (7-9 days). These data demonstrate, therefore, that prenatal stress eliminates the sex difference normally observed in pup-induced maternal behavior. Moreover, the data suggest that prenatal stress renders the male's responsiveness to young more "female-like," while conversely rendering the response of the female more "male-like."     

Maternal aggression in endothelial nitric oxide synthase-deficient mice

Lactating female rodents protect their pups by expressing fierce aggression, termed maternal aggression, toward intruders. Mice lacking the neuronal nitric oxide synthase gene (nNOS-/-) exhibit significantly impaired maternal aggression, but increased male aggression, suggesting that nitric oxide (NO) produced by nNOS has opposite actions in maternal and male aggression. In contrast, mice lacking the endothelial nitric oxide synthase gene (eNOS-/-) exhibit almost no male aggression, suggesting that NO produced by eNOS facilitates male aggression. In the present study, maternal aggression in eNOS-/- mice was examined and found to be normal relative to wild-type (WT) mice in terms of the percentage displaying aggression, the average number of attacks against a male intruder, and the total amount of time spent attacking the male intruder. The eNOS-/- females also displayed normal pup retrieval behavior. Because a significant elevation of citrulline, an indirect marker of NO synthesis, occurs in neurons of the hypothalamus of lactating WT mice in association with maternal aggression, we examined the brains of eNOS-/- females for citrulline immunoreactivity following an aggressive encounter. The aggressive eNOS-/- females exhibited a significant elevation of citrulline in the medial preoptic nucleus and the subparaventricular zone of the hypothalamus relative to unstimulated lactating eNOS-/- females. Taken together, these results suggest that NO produced by eNOS neither facilitates nor inhibits maternal aggression and that NO produced by eNOS has a different role in maternal and male aggression.     

Food restricting young hamsters (Mesocricetus auratus) affects sex ratio and growth of subsequent offspring

Trivers and Willard (1973) predicted that stressed adult female mammals may enhance their fitness by skewing offspring sex ratios and maternal investment to favor daughters. The present study investigated whether stressing young hamsters might also influence sex ratio and growth of subsequent offspring. Control females received food ad libitum (A) on Days 1-50 postpartum (AA). Experimental females were food-restricted (R) either on Days 1-25 (RA), Days 26-50 (AR), or Days 1-50 (RR) postpartum. Subjects were mated when 91-95 days old. Litter sizes and survivorship (= % litters within a treatment that contained at least one pup), sex ratio (= % males), and pup weights in the next generation were recorded every fifth day from parturition until Day 25 postpartum. Control litters contained significantly more offspring at birth than did RR litters. Sex ratio was significantly higher at birth for AA litters than for the other treatments. Postpartum sex ratio within each group remained similar to that recorded at birth. RR litters contained significantly fewer pups compared to the other three treatments from Days 5-25. RR female pups weighed significantly more at birth than their counterparts in the other treatments. Weights of males at birth were similar in all treatments. By Day 25, both male and female RR pups weighed significantly less than control, AR, and RA pups. Food restriction early in life may have long-term consequences on sex ratio and pup growth in golden hamsters.     

Postpartum,hormonal, and nonhormonal induction of maternal behavior in rats: Effects on T-maze retrieval of pups

It is known that the home-cage maternal behavior of rats which become maternal after daily pup exposure (sensitization) is almost indistinguishable from that of lactating mothers, but that sensitized and lactating rats can be distinguished by their pup-retrieval performance in a T-maze extension of the home cage. The present study explored this difference further. Postpartum mothers which could not suckle due to prior nipple removal (thelectomy) retrieved as well, if not better, than intact controls in the T-maze. Hormonal induction of maternal behavior (in ? 3 days) was carried out by hysterectomy-ovariectomy plus 100 μg/kg estradiol benzoate; the performance of these females was similar to that of the postpartum groups. In contrast, only a small percentage of the sensitized mothers retrieved in the T-maze, whether the latency to onset of their maternal behavior was long (4–10 days) or short (? 3 days). Thus, hormonal factors associated with pregnancy and/or parturition, but not suckling stimulation, may facilitate T-maze retrieval of pups. The possible ethological significance of the T-maze test as a measure of maternal responsiveness is discussed.     

Postisolation aggression and olfactory cues.

Aggressive maternal behavior was tested by placing intruders in the home cages of 210 individually housed lactating mice 3-8 days postpartum. The intruders were of 6 types: castrated males and females, intact males and females, mothers of 3-8 day old pups, and mothers of older pups. All fights were initiated by the resident lactating female. There were significantly fewer attacks on castrated males than on intact males (p less than .001), and fewer attacks on castrated females than on intact males and females (p less than .001, p less than .01, respectively). There were no attacks on mothers of 3-8 day old pups. Attacks on older mothers were significantly more frequent than on younger mothers (p less than .01). The results indicate that maternal aggression in albino mice is strongly influenced by the hormonal and reproductive state of the intruder.     

Accumbal dopamine function in postpartum rats that were raised without their mothers

Postpartum rats that had been previously raised in an artificial rearing (AR) apparatus, without their mothers or siblings during the preweaning period, show altered maternal responses towards their own offspring in adulthood. In mother-reared (MR) rats, nucleus accumbens (NAC) dopamine (DA) responses to pups evoke a robust sustained rise during the postpartum period and following treatment with estrogen/progesterone parturient-like hormones (Afonso et al., 2009). These MR females had siblings that received AR rearing with varying amounts of preweaning tactile stimulation (ARmin; ARmax). The present study examined NACshell DA responses to pup and food stimuli in these AR rats, and statistically compared them to their MR siblings. Microdialysis samples were collected from adult (90 days postnatal) AR females in different parity states (cycling vs. postpartum, Exp. 1), or after ovariectomy with different hormone treatments (sham vs. hormone, Exp. 2. After basal sample collection, pup and then food stimuli were individually presented to the females in the dialysis chamber. As with their MR siblings, basal DA concentrations were lower and pup-evoked DA responses greater in hormonally-primed AR females than in non-primed AR controls. Compared to their postpartum MR sisters (Exp. 1), AR rats had increased basal DA levels, reduced pup related DA elevations, and disrupted maternal behavior. The postpartum AR impairment in pup-evoked DA was reversed by additional pre-weaning tactile stimulation. Exogenous hormones (Exp. 2) eliminated AR impairments on pup-evoked DA responses. Although MR and AR siblings had comparable DA responses to food stimuli, upon reanalyzing MR data it was found that only postpartum dams had DA responses to pups greater than to food. These data suggest that that the hormonally induced suppression of basal DA levels may reflect saliency of pups which was greater in MR than in AR dams. Preweaning tactile stimulation could partially reverse these effects only in naturally cycling or parturient animals.     

Accumbal dopamine function in postpartum rats that were raised without their mothers

Postpartum rats that had been previously raised in an artificial rearing (AR) apparatus, without their mothers or siblings during the preweaning period, show altered maternal responses towards their own offspring in adulthood. In mother-reared (MR) rats, nucleus accumbens (NAC) dopamine (DA) responses to pups evoke a robust sustained rise during the postpartum period and following treatment with estrogen/progesterone parturient-like hormones (Afonso et al., 2009). These MR females had siblings that received AR rearing with varying amounts of preweaning tactile stimulation (ARmin; ARmax). The present study examined NACshell DA responses to pup and food stimuli in these AR rats, and statistically compared them to their MR siblings. Microdialysis samples were collected from adult (90 days postnatal) AR females in different parity states (cycling vs. postpartum, Exp. 1), or after ovariectomy with different hormone treatments (sham vs. hormone, Exp. 2. After basal sample collection, pup and then food stimuli were individually presented to the females in the dialysis chamber. As with their MR siblings, basal DA concentrations were lower and pup-evoked DA responses greater in hormonally-primed AR females than in non-primed AR controls. Compared to their postpartum MR sisters (Exp. 1), AR rats had increased basal DA levels, reduced pup related DA elevations, and disrupted maternal behavior. The postpartum AR impairment in pup-evoked DA was reversed by additional pre-weaning tactile stimulation. Exogenous hormones (Exp. 2) eliminated AR impairments on pup-evoked DA responses. Although MR and AR siblings had comparable DA responses to food stimuli, upon reanalyzing MR data it was found that only postpartum dams had DA responses to pups greater than to food. These data suggest that that the hormonally induced suppression of basal DA levels may reflect saliency of pups which was greater in MR than in AR dams. Preweaning tactile stimulation could partially reverse these effects only in naturally cycling or parturient animals.     

Effects of prolonged estrogen-progesterone treatment and hypophysectomy on the stimulation of short-latency maternal behavior and aggression in female rats

Two experiments were undertaken to examine the stimulation of home-cage and/or maternal aggressiveness by a hormonal treatment stimulating short-latency maternal behavior. Nonpregnant ovariectomized rats were treated with a 16-day regimen providing pregnancy levels of estrogen (E, 5-mm Silastic capsule) and progesterone (P, daily injection of 4 mg) followed by E and P withdrawal, with or without a terminal injection of estradiol benzoate (EB, 5 micrograms/kg). In Experiment 1, hormonally treated and control females were exposed continuously to pups and tested for aggression toward male intruders on the fifth day of pup exposure. Females receiving E/P/Oil and E/P/EB were highly aggressive whether or not they had yet shown maternal behavior, whereas vehicle-treated females were nonaggressive. In Experiment 2, hypophysectomized (HYPX) and Sham-HYPX females received either E/P/EB or a control treatment and were tested with male intruders (a) immediately preceding and (b) on the fifth day of continuous pup exposure. HYPX and Sham-HYPX females treated with E/P/EB were almost equally aggressive both preceding and following pup exposure (during which they initiated maternal care), whereas HYPX and Sham-HYPX vehicle-treated females were nonaggressive at both tests. In contrast, maternal behavior latencies were reduced by E/P/EB only among Sham-HYPX females. The results establish that an E/P/EB-treatment which elicits short-latency maternal responses also increases aggressiveness toward intruders. Pituitary products, although involved in the mediation of maternal responsiveness, do not contribute significantly to the stimulation of female aggressiveness by ovarian hormones.     

Fertility of the early postpartum, lactating domestic rabbit

Sixty-four crossbred primiparous lactating does each suckling six pups were allocated at random into four groups and were mated on either Day 1, 2, 3, or 4 post partum (where Day 0 = the day of parturition). They were subsequently killed on Day 10 post coitum (where Day 0 = the day of mating) to assess fertility. There were no significant differences between treatment groups in their mating response (97% overall), ovulation response (77% overall), implantation response (83% overall), implantation rate (8.7 overall), or preimplantation mortality rate (24% overall). Ovulation rate was significantly increased in does mated on Days 3 and 4 (13.3 and 13.1, respectively), compared with those mated on Day 1 (10.2, P<0.05) and Day 2 (9.6, P<0.01) post partum. From these results we conclude that fertility is high throughout the early postpartum period in the lactating rabbit.     

Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus

Adult male and female white-footed mice (Peromyscus leucopus) and deermice (P. maniculatus) from sympatric populations commit infanticide on neonates of either species. A laboratory experiment was conducted to determine whether aggression in maternal females could effectively deter infanticidal intruders. Females of both species exhibited post-partum aggression and dominated intruders of either sex or species in 83 of 88 trials. In the absence of the mother, neonates were attacked by intruders in 82 out of 84 trials. Maternal females were considerably more aggressive than anoestrous females. The implications for female territorially as a mechanism to prevent infanticide are discussed.