On the dual nature of maternal aggression in rats

Presentation of a natural predator, a cat, was used to differentiate elements of maternal attack by female rats on a male intruder. Following exposure (without direct physical contact) of post-partum females to a cat or to a toy stuffed cat (control group), the females were replaced in their home cages and presented with a male intruder rat. Cat exposure reliably decreased lateral attack to the intruder, as well as locomotion, but had no effect on either jump attack or an upright defensive posture (boxing). Since predator exposure produces a somewhat durable increase in defense, along with inhibition of nondefensive behavior, these results suggest that maternal aggression represents a mixture of offensive, usually related to competition, and defensive (protective) behaviors. The results indicate that maternal aggression, as a parental care behavior, appears to be at least partially resistant to fear. © 1996 Wiley-Liss, Inc.     

Relationship between maternal aggression and maternal care in the rat

Aggression among female rats is almost entirely confined to the period of late pregnancy and lactation. Behaviorally it is similar to the aggression of males including piloerection and lateral attacks, but it differs in its function. Unlike male aggression which serves to establish a social hierarchy and a territory, i. e., is competitive, maternal aggression is protective, i. e., it serves to prevent predation of the mother's offspring. In this respect it is closely related temporally and causally to maternal care; if the offspring are removed maternal aggression wanes almost immediately–its function no longer exists! Studies on aggression by mothers, among rats, from the author's laboratory are reviewed and comparisons made with maternal care. As noted, maternal aggression and maternal care are closely related during the cycle of maternal behavior and they share a similar hormonal basis and possibly the effect of uterine stimulation, but maternal care requires prolactin and the decline of progesterone while maternal aggression appears independent of pituitary hormones and does not require a decline in progesterone. Maternal aggression like maternal care appears to be organized into a hormonal phase, during pregnancy, parturition, and for about a week postpartum and a nonhormonal phase thereafter. Bilateral radiofrequency lesions of the lateral midbrain peripeduncular nucleus (PPN) produce deficits in maternal aggression if made on lactation day 7 (L7), but not earlier, without producing significant deficits in maternal behavior. Experiments showed that the PPN does not mediate hormonally stimulated maternal aggression; it appears to mediate only nonhormonally stimulated maternal aggression. Studies on the role of pregnancy hormones on long-term retention of maternal aggression and the role of olfaction in maternal aggression are also reviewed. © 1994 Wiley-Liss, Inc.     

Defensive behaviors in rats following septal and septal--amygdala lesions

Rats with anterior septal lesions showed a pattern of consistent enhancement of defensive behaviors normally elicited by threatening conspecifics, with no enhancement of attack or general reactivity. Further division of this group indicated that damage to sites anterior and ventral to the septal area, sites previously implicated in the "septal syndrome," produces maximal effect on these behaviors. When amygdala lesions are combined with septal damage this enhanced defensive responding is almost completely eliminated. These results were interpreted as indicating that the septal syndrome represents hyperdefensiveness to conspecific threat stimuli rather than aggression or increased general reactivity, and that amygdaloid mechanisms are also involved in the regulation of conspecific defensive behaviors.     

Sensory control of maternal aggression in Rattus norvegicus

Female rats become aggressive toward adult conspecifics during lactation. This change in social affect is dependent on the presence of the offspring, because maternal aggression disappears when the pups are removed. It was found that a similar decline occurs when the litter is placed in a glass flask while remaining in the home cage. In contrast, maternal aggression persists following placement of the pups in a nylon mesh bag. The pups did not vocalize while being in the mesh bags, so it appears that olfactory cues from the offspring constitute a critical element in the maintenance of maternal aggression in the rat. It has been suggested that the odor not only of the pups but also of the intruder may contribute to eliciting aggressive behavior in lactating rodents. In line with this proposal, it was found that mother rats spend about one third of the time preceding the first attack sniffing the body of the intruder. In contrast to findings in mice, housing of the prospective intruder behind a double wire mesh partition in the lactating female's home cage failed to reduce her aggressiveness toward him. Rats, then, may require more intimate contact with an individual than do mice for the aggression-reducing effect of familiarization to be observed.     

The offensive nature of maternal aggression in mice: Effects of fluprazine hydrochloride

The phenylpiperazine fluprazine hydrochloride was used to test the hypothesis that maternal aggression in laboratory mice reflects offensive motivation. Lactating females (n = 8 per condition) tested for aggression following drug treatment (1.0 mg/kg and 5.0 mg/kg of fluprasine) were significantly less aggressive than saline controls according to all measures used. The findings support the hypothesis that maternal aggression is offensive in nature, and provide no evidence that maternal attack is a mixture of offensive and defensive tendencies.     

Intergenerational effects of cocaine on maternal aggressive behavior and brain oxytocin in rat dams

Gestational cocaine treatment results in significantly increased maternal aggression towards an intruder by postpartum day six, while acute postpartum treatment dose dependently decreases maternal aggressive (MA) behavior. Both increased and decreased aggression in the cocaine-treated dams are correlated with either decreased or increased levels of oxytocin in the amygdala, respectively. The current study was an effort to determine whether the effect of gestational cocaine on maternal aggression is transient or would continue into the postpartum period; whether an intermittent cocaine treatment regimen, which incorporates gestational and postpartum intermittent cocaine treatment, would differ from chronic daily gestational treatment; and finally, whether next generation female offspring of cocaine-treated or control dams would have altered MA behavior and oxytocin system changes attributable to either prenatal drug exposure, rearing condition or both. We now report no increase in maternal aggression following chronic gestational treatment and significantly lower levels of aggression in intermittently treated dams on postpartum day eight, with no significant effects in either group on postpartum day 12. Young adult female offspring of the cocaine-treated and control dams, who reared their own natural litters and were tested on postpartum day eight for maternal aggression, had higher levels of maternal aggression towards an intruder attributable to both prenatal cocaine exposure and rearing condition. Higher aggression in cocaine-reared next generation dams was associated with lower levels of oxytocin in the amygdala. Intergenerational effects of cocaine were apparent with respect to aggression and oxytocin system changes.     

Factors influencing maternal attack on conspecific intruders by lactating female “TO” strain mice

Factors regulating maternal attack in “TO” strain mice were investigated to determine 1) optimal conditions for inducing this behaviour and 2) the likely utility of this activity. Lactating females were more likely to attack male intruders than female intruders. The mate's presence reduced maternal attack in this strain, or (putting it conversely) aggression was generated in the male's absence. Removal of the mothers from their litters for four to five hours also suppressed maternal attack. Investigation of the bite targets in the maternal attack suggested that it is a defensive, rather than an offensive, response.     

Offensive and defensive bite-target topographies in attacks by lactating rats

The attacks by resident lactating Wistar rats on sexually naive conspecifics of both sexes were examined. Male and female intruders were equally attacked in terms of frequency and number of bites, but the topographies of biting seen in these encounters were different. Similarly to male-male agonistic interactions, females were attacked in a fashion which avoided bites to the head and snout (“offensive” attack), whereas males were frequently bitten on such vulnerable regions (“defensive” attack). This dichotomy in bite pattern suggests that different motivations and functions underlay maternal aggression in these situations. The defensive attack on males may be a deterrent to infanticide since only male intruders counterattack lactating females and kill their pups. The attack on females may be concerned with resource competition.     

Extracellular amino acid levels in the paraventricular nucleus and the central amygdala in high- and low-anxiety dams rats during maternal aggression: regulation by oxytocin

Brain oxytocin (OT) regulates aspects of emotionality and stress coping including maternal behavior and maternal aggression. Maternal aggression correlates with the amount of OT released within the paraventricular nucleus (PVN) and the central amygdala (CeA). OT, a key neurotransmitter or neuromodulator, is likely to modulate other neurotransmitter systems. Here, we investigated the dynamic changes in extracellular concentrations of the amino acids aspartate, glutamate, gamma-aminobutyric acid (GABA), serine, histidine, arginine and taurine in the PVN and CeA in lactating rats bred for high (HAB) and low (LAB) anxiety-related behavior under basal conditions and during maternal aggression. Further, to determine whether local OT is involved in the regulation of amino acid release we infused a selective OT receptor antagonist (OTA) via local retrodialysis. Within the CeA, HAB and LAB dams differed in the basal release of glutamate and arginine. Infusion of a selective OTA increased the concentrations of glutamate and aspartate in LAB dams and GABA in HAB dams. In OTA-treated HAB and LAB dams taurine levels increased during maternal aggression. Within the PVN, the highly-aggressive HAB dams showed a more pronounced increase in aspartate and serine levels; the latter being attenuated by local OTA administration. However, OTA did not affect the level of any amino acid in the LAB dams. Thus, the extracellular concentrations of selected amino acids differed between lactating HAB and LAB dams under both basal conditions and following maternal aggression. The effects of OT within the CeA and PVN on maternal aggressive behavior might be related to its regulation of local amino acid release.     

Effects of daily and acute restraint stress during lactation on maternal aggression and behavior in mice

A decreased reactivity to stressors during lactation might heighten the expression of maternal care (including defense of offspring) by minimizing the extent to which stress can impact maternal care. Although stressors applied during pregnancy have variable effects on maternal aggression (or defense of offspring), to date no study has examined the effects of stress applied during the postpartum period on maternal aggression. In this study, we examined the effects of both daily and acute restraint stress (30 min) applied postpartum on maternal aggression and other maternal behaviors. Daily restraint (ending 2 h before testing) did not alter any measure of maternal behavior, including nursing, licking and grooming of pups and pup retrieval, or any measure of maternal aggression. In contrast, acute stress significantly impaired total time aggressive and number of attacks, but pup retrieval was normal. c-Fos levels were significantly elevated in a number of brain regions in association with acute stress, including lateral septum (LS), caudal periaqueductal gray and medial amygdala (MeA), suggesting possible sites where stress reactivity could alter aggression. Together, the results indicate that acute restraint stress impairs maternal aggression and provide a starting point for future studies examining how stress reactivity pathways may intersect with maternal aggression pathways.     

Offensive and defensive aggression in humans: A longitudinal perspective

Offensive and defensive aggression were distinguished on the basis of associated events. Behavior delivering noxious stimuli was defined as defensive when it was a response a threatening situation and as offensive when it was an unprovoked act. The existence of a general aggression factor was implied by the finding that initiators of aggression also readily defend themselves if attacked. The use of a peer nomination and teacher rating variable for offensive aggression, “Attacks without reason, teases others, naughty things”; and another for defensive aggression, “Defends him/herself if teased, but does not tease or attack others without reason,” yielded differential results. Offensive aggression at age 14 was significantly predicted by aggressive behavior age 8, while defensive aggression was not. Intercorrelations of rating variables at 14 showed that offensive aggression was related to weak self-control and defensive aggression to strong self-control. Only offensive aggression at age 14 predicted criminality at age 20. The results indicate a diversity of motivations for aggressive behaviors, as suggested by observations on animal behavior.     

Maternal aggression: disruption by perioral anesthesia in lactating Long-Evans rats (Rattus norvegicus)

Role of perioral somatosensation in the display of maternal aggression in Long-Evans Norway rats (Rattus norvegicus) was investigated during early lactation by local anesthesia of the mystacial pads with lidocaine, which blocks conduction in the infraorbital nerve. Acute perioral anesthesia markedly reduced the likelihood that maternal aggression was expressed; this effect of perioral anesthesia was not ameliorated by a repeated test with the same treatment or by pretreatment fighting experience. The dams that fought with the intruder during perioral anesthesia did so after greatly increased sniffing contact and with decreased vigor compared with controls. Males that were attacked tended to freeze, whereas males that were not attacked were active. Thus, trigeminal afferents are critical for the initiation and normal execution of maternal aggression responses in Norway rats.     

Effects of chronic social stress during lactation on maternal behavior and growth in rats

Maternal mood disorders such as depression and chronic anxiety can negatively affect the lives of not only mothers, but also of partners, offspring, and future generations. Chronic exposure to psychosocial stress is common in postpartum mothers, and one of the strongest predictors of postpartum depression is social conflict. The objective of the current study was to evaluate the effects of chronic social stress (CSS) during lactation on the maternal behavior (which consists of maternal care and aggression toward a novel conspecific) of lactating rats, as well as on the growth of the dams and their offspring. It was hypothesized that chronic daily exposure to a novel male intruder would alter the display of maternal behavior and impair growth in both the dam and offspring during lactation due to the potentially disruptive effects on maternal behavior and/or lactation. The data indicate that CSS during lactation attenuates maternal care and the growth of both dams and pups, and increases self-grooming and maternal aggression toward a novel male intruder. These results support the use of CSS as a relevant model for disorders that impair maternal behavior and attenuate growth of the offspring, such as postpartum depression and anxiety.     

Maternal aggression in mice: Protection of young is a by-product of attacks at the home site

Lactating female mice attacked male intruders in their home cages but showed little attack behavior either in novel cages or in cages with which they had been familiarized. Presence or absence of young did not determine the occurrence of maternal aggression, whereas attacks on the young by the intruder decreased maternal aggression and increased cannibalism of pups by the dams. Apparently, if the function of maternal aggression in mice is protection of the young, such protection occurs because the pups are in a place where attacks are likely to occur and not because the dam “defends” the young.     

Influence of timing of post-weaning isolation on play fighting and serious aggression in the male golden hamster (Mesocricetus auratus)

Effects of timing of social isolation on play fighting and serious fighting were studied at different ages in male golden hamsters. Litters were isolated at 21, 35, and 65 days of age, and tested in a resident-intruder paradigm. Behaviors were compared within grous and with a fourth group of socially reared conspecifics. The earlier the pups were isolated, the more they engaged in play activities. Later, in adulthood, the aggression level of the same animals was retested using the same paradigm. The three isolated groups showed a high level of aggression, with significant differences among them. When compared with socially reared subjects, a reliable difference in the level of aggression was also found. These results support the view that early social experience is important, suggesting that isolation during early critical periods of socialization has a significant impact on play fighting, whereas short periods of isolation may be enough to trigger adult agonistic behavior. © 1994 Wiley-Liss, Inc.     

Exposure to maternal vs. paternal partner violence,PTSD, and aggression in adolescent girls and boys

Adolescents who witness interparental violence (IPV) are at increased risk for perpetrating aggressive acts. They are also at risk for post‐traumatic stress disorder (PTSD). In this study, we examined the relation between exposure to maternal vs. paternal physical IPV and adolescent girls' and boys' aggressive behavior toward mothers, fathers, friends, and romantic partners. We also assessed the influence of PTSD (as assessed by the Diagnostic Interview for Children and Adolescents‐IV (DICA‐IV)) on the relation between exposure to IPV and aggressive behavior. Participants were 63 girls and 49 boys, ages 13–18, consecutively admitted to a youth correctional facility or assessment facility designated to serve aggressive and delinquent youth. Structural equation modeling was used to estimate unique relations between exposure to maternal vs. paternal IPV and youth aggression in relationships. Girls who observed their mothers' aggressive behavior toward partners were significantly more aggressive toward friends. Similarly, boys who witnessed their fathers' aggression were significantly more aggressive toward friends. Adolescent girls and boys who observed aggression by mothers toward partners reported significantly higher levels of aggression toward their romantic partners. Approximately one third of our sample met PTSD criteria; the relation between exposure to parental IPV and aggression was stronger for individuals who met criteria for PTSD. The implications of understanding the relations between parents' and their daughters' and sons' use of aggression are discussed within the context of providing support for families in breaking intergenerational patterns of violence and aggression. Aggr. Behav. 32:385–395, 2006. © 2006 Wiley‐Liss, Inc.     

The effects of negative reinforcement for irritable aggression on resident-intruder behavior

This experiment demonstrated that rats trained to display elevated levels of shock-induced aggression in a negative reinforcement paradigm displayed more boxing behavior than yoked control groups in a later test in which intruder rats were placed in the home cage of resident rats. Resident or intruder status did not affect the influence of the negative reinforcement procedure on the observed resident-intruder behavior of trained animals; however, naive intruders paired with trained residents displayed increased defensive behavior, suggesting that negative reinforcement for shock-induced aggression affected the behavior of these residents.     

High maternal aggression in dwarf hamsters (Phodopus campbelli and P. sungorus)

The defense of offspring, termed maternal aggression, is a highly conserved behavior in mammals, including rodents. This study examined relative levels of maternal aggression in two closely related dwarf hamster species, Phodopus campbelli and P. sungorus, that normally inhabit high latitude, boreal environments. When tested with first litters and with the breeder male remaining with the female (for P. campbelli the male is necessary for successful rearing of offspring), both species exhibited high levels of maternal aggression with average duration of aggressive behavior>80 sec for a 10 min test. For P. sungorus, males are not required to rear offspring. P. sungorus females with either one or multiple litters (singly housed after impregnation) exhibited significantly higher levels of aggression (>300 sec) relative to females co‐housed with the sires. In terms of species differences in attack style, P. campbelli exhibited a boxing or clawing strategy for ～50% of total attack time, but for P. sungorus, this form of attack occurred<5% of the time. For P. sungorus, attacks to the vulnerable belly and flank constituted>90% of all attacks, but these regions were attacked ～50% of the time for P. campbelli. A survey of levels of maternal aggression of rodents in other genera suggests that maternal aggression in Phodopus is at the high end of the spectrum. Results of this study suggest that the presence of the breeder male may actually suppress aggression in P. sungorus. This fact, as well as its high level of aggression and its distant relationship to mice and rats, suggest P. sungorus as a possible model for future studies on the neurobiological basis of maternal aggression. The relationship between the high rates of maternal aggression and life history strategy in Phodopus is discussed. Aggr. Behav. 00:000–000, 2005. © 2005 Wiley‐Liss, Inc.     

Does fear modulate defensive and offensive types of maternal attack in mice?

Swiss CD‐1 lactating mice show a different pattern of attack toward intruders of differing sex, displaying defensive attack against the male (bites on the head and ventrum associated with fear) and offensive attack against the female (bites on the back and flanks with no elicitation of fear). This dichotomy may reflect diverse functions of maternal aggression: the attack toward males (the more infanticidal gender in laboratory strains) has been interpreted as a counterstrategy to infanticide, whereas the attack toward females may serve to establish a social hierarchy or to space rivals of the same sex. In terms of proximal mechanisms, fear may be a key factor involved in the modulation of the different patterns of attack. In Experiment 1 we compared the pattern of attack of lactating females in Swiss CD‐1 and Wild mice toward male and female intruders in relation to fear components of behavior of the attacking dams. Results showed that in Swiss mice, male intruders were attacked with a defensive type of attack accompanied by high levels of fear, whereas female intruders did not elicit fear in the attacking animal but were attacked with an offensive pattern. In Wild mice, both types of intruders were attacked with a defensive pattern; notwithstanding, fear was evident only toward male intruders. This suggests that fear is not totally responsible for the expression of the defensive type of attack. To test the hypothesis that defensive attack toward male and female intruders may be related to the infanticidal potential of the intruder, Experiment 2 examined levels of infanticide in both male and female Swiss CD‐1 and Wild mice. Swiss female mice showed virtually no infanticidal behavior, whereas Swiss males and both sexes of Wild mice showed similarly high levels of infanticide (55%–75%). From a game theory perspective, the defensive pattern of maternal attack toward female intruders in Wild mice is discussed as “extreme” defense of a high value resource and thus, functionally, a competitive form of aggression. Aggr. Behav. 26:193–203, 2000. © 2000 Wiley‐Liss, Inc.     

Conspecific aggression influences food carrying: Studies on a wild population of Rattus norvegicus

Laboratory rats, like many other animal species, transport food. Their behavior is influenced by factors such as food size, the time required to eat, travel distance, travel difficulty, and the availability of cover, etc. Recent versions of optimal foraging theory suggest that species that display such behavioral patterns do so in order to minimize risk to predation while at the same time maximizing food gain. Nevertheless, it is not clear that this explanation applies to rats, nor is it easy to investigate this problem in a laboratory. The results of the present study on urban feral rats show that their food handling behavior is similar to that of domestic rats. The results also suggest that food carrying can serve defensive as well as communicative functions. Aggression around food sources was high. Smaller rats always carried food and some large rats infrequently carried food, suggesting that the food carrying by smaller, subordinate rats may help them avoid conspecific aggression. The rats also vigorously attempted to steal food that was carried home by conspecifics. This result suggests that food carrying can redistribute food resources and inform conspecifics about food availability. The results demonstrate the utility of multilevel behavioral analysis and also demonstrate that for rats, food transport has functions other than predator avoidance, including avoidance of conspecific aggression and communication about food availability. © 1996 Wiley-Liss, Inc.