Colony aggression in laboratory rats: A review and some recommendations

The behavioral response of established colonies of domesticated rats to the presence of an unfamiliar intruder of the same species represents one of the most effective procedures yet developed to study aggression in the laboratory. Here, the social, experiential, and environmental variables that influence attack severity are reviewed and several important methodological issues are discussed. Brief exposures of intruders to intact colonies may produce misleading results but long-term test sessions increase the likelihood that intruders will be either killed or severely injured. We describe a simple modification of the colony-intruder procedure whereby intruders can successfully defend themselves during long sessions and thus reduce serious injury. The modified procedure appears to conform more closely to what happens during aggressive encounters in free-living populations of wild rats.     

Situational Support,Privacy Regulation,and Stress

There is substantial evidence that people have difficulty asking someone to leave in order to obtain solitude. This study evaluated the hypotheses that (a) people regulate privacy to the extent that they feel supported by the social and physical environments, (b) people who reject an intruder will cite situational pressures that legitimize their behavior, (c) rejecting an intruder can itself be stressful, but (d) verbalizations that legitimize regulation can help pevent or reduce the stress. Participants were performing a task that required solitude when confronted with an intruder. Social/normative (informative signs) and environmental (visitor's chair placement) cues favoring or opposing regulation of the intruder were manipulated in a 2 x 2 factorial design. As hypothesized, participants were most likely to reject the intruder if they had both environmental and informational support for doing so. People generally cited task pressures when confronted with the intruder, but when the sign and the chair supported regulation, they cited the task less and the situation (especially the chair) more. There was little support for the hypothesis that regulating an intruder without situational support would be stressful; however, verbal justification for regulation (i.e., citation of more external pressures) was generally related to lower indices of stress. The results support the idea that people read and use situational cues when controlling their solitude.     

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.     

Septal lesions and biting attacks in rats bidirectionally selected for emotionality

Twenty-nine colonies composed of one female and two male rats of high or low emotional strain were established. A dominant male of each colony was identified based on its attacks on an intruder rat. It was found that dominant males of the low emotional strain colonies were significantly more aggressive than those of the high emotional strain. Septal lesions or sham operations were given to dominant males of both strain colonies. Intruder tests were followed and several aggressive behaviors were measured by VTR observation. Biting attacks of the high emotional strain decreased for 10 days after septal latencies were shortened by septal lesions. Lesions X Strain interaction was significant. These results suggest that septal lesion effects on biting attacks are influenced by artificial genetic operations.     

Behaviour of Young Growing Pigs in a Resident‐Intruder Test Designed to Measure Aggressiveness

A total of 125 growing pigs (47 days old) were tested for aggressive responses on two occasions using a resident‐intruder (R‐I) design. Our aims were twofold: (1) to attempt to replicate earlier work on pigs showing that resident aggression is a consistent individual characteristic, unaffected by weight or sex of the resident or intruder and (2) to develop behavioural measures to characterise the wide range of aggressive responses in the test. Resident pigs, housed since birth with littermates, were placed individually in a divided‐off portion of their home pen, and a smaller, unfamiliar intruder (approximately 66% of the resident's weight) was introduced. The test ended 5 min after the first investigation of the intruder by the resident or when one of the pigs began to attack the other (by delivering a sudden, rapid series of bites). On days 1 and 2, 33.6% and 43.2% of tests, respectively, ended in an attack by a resident. Intruder attacks were rare. Pigs were consistent in whether they attacked or not over the two tests, although attack latencies for pigs attacking in both tests were not correlated. Females were more likely to attack and attacked more quickly than males on the first test day but not in the second test or overall. Intruder sex had some effect on the test outcome (males were attacked more rapidly in the second test only). Resident and intruder weight had no effect. Aggressive pigs (meaning pigs that attacked vs. pigs that did not and fast‐attacking pigs vs. slow‐attacking pigs) showed a number of differences in behaviour during the R‐I test: (1) they took longer to make initial contact with the intruder in their first test; (2) they showed a higher frequency of aggressive acts (single head knocks, bites, and shoves); (3) they spent a greater proportion of the test engaging in social contact with the intruder rather than non‐social behaviours; (4) their social behaviour involved more postures directed toward the head as opposed to flank‐ or rear‐directed postures or re‐establishing social contact; and (5) they showed closer physical contact with intruders during social encounters, as characterised by their lower head positions. Some of these behavioural measures could be used to improve the measuring power of the test in the future. Improved behavioural measures would enable aggressiveness scoring among pigs that did not attack instead of classifying them all together as “non‐attacking.” Aggr. Behav. 28:401–415, 2002. © 2002 Wiley‐Liss, Inc.     

Socially induced renal pathology of captive wild rats (Rattus villosissimus)

Long-haired rats, Rattus villosissimus, were studied in large cages. Groups of adult rats (each of 3 males, or 1 male and 2 females) were observed during intermittent encounters with a male intruder for up to 9 days. Two further groups, each of 8 males and 8 females, were maintained for 70 days without introduction of intruders. Controls were kept in small cages in which intolerant behavior was rare. Behavior during attack resembled that of male R. norvegicus, but social relationships were less stable. Only observations on males are described in detail. Some rats collapsed under attack, though unwounded, and died when not removed. Collapse occurred sometimes after a few hours, but sometimes after many days of exposure. Exposure to attack was accompanied by a decline in body weight and by some adrenal hypertrophy. Two kinds of renal pathology are described: focal glomerular hypercellularity (FGH), probably due to glomerulonephritis, and dilated distal convoluted tubules. Neither condition occurred in the controls. FGH occurred in 3 of 12 rats (25%) that remained apparently healthy during the 9 days of continuous exposure, in 21 of 23 intruders (91%) that were exposed to intermittent attack over 9 days or less without becoming debilitated, and in 8 of 11 such rats (73%) that collapsed. All rats examined from 70-day colonies had FGH, whether collapsed or not. Dilated tubules occurred in 6 of 32 intruders (19%) exposed to intermittent attack, and in 2 of 6 animals that collapsed during 70 days of exposure. Renal pathology, especially glomerulonephritis, was therefore a correlate of social intolerance; but there was no evidence that it was a significant cause of death.     

Enhanced social docility in male hooded rats by dermal cautery of the vibrissal pads

Ablation of the vibrissal pads in rats causes subsequent deposition of scar tissue with little or no regrowth of the vibrissae. Cauterized and intact mature male Long Evans rats were tested for shockelicited fighting, mouse killing, and colony intrusion forms of laboratory-induced aggression. The results revealed that only conspecific social fighting is blocked by ablation of the major vibrissal follicles. Although no significant group differences were noted in tests for mouse killing, shock-elicited paired fighting and territorial defense against a strange intruder were minimal in cauterized groups. The results emphasize the importance of specific sensory experience in reference to distinct forms of aggressive responding and support a new experimental technique for further investigation of sensory interactions with sources of aggressive behavior.     

Enhanced defense in adult rats deprived of playfighting experience as juveniles

In an earlier study we found that shock-elicited defensive aggression was intensified in rats that had been deprived of playfighting as juveniles. The three experiments reported here extend this phenomenon to the more naturalistic intruder/resident paradigm for eliciting defense. Rats were reared from 20 to 50 days in one of three conditions: in pairs or in isolation with or without 1 hour of daily playfighting experience. They were rehoused in small groups at 50 days, when the frequency of play is beginning to wane, in order to eliminate the effects of ongoing isolation at the time of testing. They were tested for defense at 80 to 100 days by being placed in a resident's cage for 10 minutes. Our main finding was that play-deprived animals spent significantly more time immobile after they had been attacked than did animals of the other two groups. The increased immobility associated with playfighting deprivation is not caused by baseline differences in emotionality such as those elicited by a novel environment (Experiment 1), the presence of a strange animal (Experiment 2), or nonsocial aversive stimuli (Experiment 3). Furthermore, play-deprived rats were not more reactive when pinched with forceps to stimulate a bite delivered by a conspecific, whether or not another rat was present behind a divider. Thus isolates' greater reactivity may be restricted to situations involving pain coupled with close proximity to and contact with another rat. A secondary finding was that there were no differences in defensive behaviors other than immobility. The appropriate generalization to be drawn from these studies is that early social deprivation facilitates the defensive response to a social threat that happens to be prepotent under the given experimental conditions.     

Defeat-induced hypoalgesia in the rat: effects of conditioned odors, naltrexone, and extinction

In Experiment 1, male rats were either defeated as a colony intruder by alpha conspecifics or had no defeat experience, and 24 hr later they were given a paw injection of formalin prior to observational tests with or without alpha-colony odors. The combination of defeat and tests with these odors produced conditioned hypoalgesia (i.e., a suppression in paw licking) and freezing. In Experiment 2, defeated rats were given either an injection of naltrexone or saline prior to defeat and 24 hr later prior to testing. An injection of naltrexone prior to defeat increased freezing during defeat and later testing. In contrast, naltrexone during testing did not affect freezing but significantly reduced hypoalgesia. In Experiment 3, a 12-hr exposure session with alpha-colony odors extinguished hypoalgesia in previously defeated rats. These findings are discussed in terms of associative, opioid/nonopioid, and adaptive evolutionary processes.     

Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus)

This investigation was concerned with the identification of the ultrasonic vocalizations produced by intruders during aggressive interactions and the role of these signals in agonistic behavior of rats. In the first experiment, experienced resident males were paired with both devocalized and intact vocalizing naive intruder males. Devocalization of the intruder males resulted in a drastic decrease in 50-kHz vocalizations and the elimination of all 22-kHz vocalizations. This almost total absence of ultrasonic vocalizations was not accompanied by any change in resident aggressive behavior or intruder defensive and submissive behavior. In a second experiment, naive intruders were tested with either deafened or intact resident males. Similarly, preventing residents from hearing intruder ultrasounds had no detectable effect on any aggressive behavior. These experiments are not consistent with the correlative evidence that intruder-produced 22-kHz vocalizations inhibit the aggressive behavior of the resident. The results also show that most of the ultrasonic vocalizations emitted during aggressive encounters are probably produced by the intruder.     

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 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.     

Consistency of aggressive temperament in domestic pigs: The effects of social experience and social disruption

Resident‐intruder (R‐I) tests can be used to measure the aggressive temperament of domestic pigs (Sus scrofa), and have previously been shown to predict the severity and persistence of aggression when unfamiliar pigs are mixed. To study the consistency of individual differences in aggressiveness over time, 112 pigs (eight from each of fourteen litters) were given two R‐I tests at each of three ages (46, 80, and 113 days). Pigs were R‐I tested singly in an arena within the home pen, where a smaller unfamiliar intruder pig was introduced to a resident pig. Latency to the first attack by the resident was recorded, and the test was stopped as soon as an attack occurred, otherwise the test lasted five minutes. Pigs from eight of the litters used here had been allowed to mix with another litter prior to weaning (days 10–30; socialised), while pigs in six litters remained in littermate groups (control). To determine whether consistency would survive the effects of social disruption, pigs were mixed into new groups on two occasions between the first and second test, then remained in these groups until the third test. Evidence of consistency was found, despite the social disruption. Socialised pigs were more aggressive than controls, females were more aggressive than males, and certain litters were more aggressive than others. After adjusting for these, consistent differences between individuals were still evident. Consistency was higher between the second and third tests compared to the first and second, possibly because of stable group membership or the effects of age or experience. In support of the idea that social experience improves consistency, socialised pigs were more consistent than controls throughout. Evidence of consistent individual differences in aggressive temperament suggests that breeding or changes to early life experiences could have a long‐lasting influence on aggressive behaviour in pigs. Aggr. Behav. 30:435–448, 2004. © 2004 Wiley‐Liss, Inc.     

Anxiolytic effects of repeated victory in male Wistar rats

Recurring evidence suggests that social stress has anxiogenic‐like effects in laboratory rodents. However, despite the fact that competitive situations are stressful, success in competitive situations reduces anxiety in humans. The aim of the present study was to investigate whether repeated experience of winning in aggressive encounters affects anxiety measures in laboratory rodents. Male rats were housed together with a female for 2 weeks. Cohabitation with females was necessary to induce high levels of aggressiveness in these animals. During the second week, half of the male rats were exposed daily for 30 min to an intruder of smaller size, and the other half remained undisturbed in their home cage. Group‐housed male rats were also used as controls. Residents attacked and defeated intruders, who did not retaliate. After the fifth encounter, all animals were tested for anxiety on the elevated plus‐maze. Repeated victory lowered anxiety measures considerably, despite the fact that aggressive encounters are stressful even for the victor. It is concluded that repeated victory has an anxiolytic action in male rats. The similarities with human data suggest that repeated winning in rats can be used as a laboratory model for success‐induced changes in human anxiety. Aggr. Behav. 26:257–261, 2000. © 2000 Wiley‐Liss, Inc.     

Pregrouping aggression and defense scores influences alcohol consumption for dominant and subordinate rats in visible burrow systems

Five male/two female rat colonies were established in visible burrow systems, with males selected for pregrouping attack scores and also evaluated in open field and cat odor tests. Dominant-subordinate pregrouping attack differences suggested that the males becoming dominant are those showing more persistent and higher level attack. For six colonies showing dominant-subordinate behavioral differences, pregrouping defense tests failed to predict subordinate status. However, pregrouping defense scores were reliably correlated with subordinate pre-postgrouping change scores for voluntary ethanol consumption. Subordinates showed higher ranked ethanol consumption than dominants, but these groups were not different on pregrouping ethanol consumption. Subordinate postgrouping ethanol consumption was positively correlated with pregrouping attack toward an adult intruder, consonant with previous findings that highly aggressive subordinates are the targets of more intense attack by dominants. These results provide further support for a view that subordination stress increases voluntary ethanol consumption in male rats and suggest some additional individual differences factors that may be involved in increased ethanol consumption for male subordinates. © 1992 Wiley-Liss, Inc.     

Aggressive behaviour elicited in rats by different social situations. Analysis of aggressive patterns and individual differences

In the present work, we have analyzed aggressive patterns shown by rats reared in different social situations. The mixed colonial group shows significantly lower scores in those behaviour patterns which are grouped in the Physical Attack factor, and mixed colonial rats are the ones that score highest in those behaviour patterns which are grouped in the Expectancy factor. Thus, these animals are the ones that show more Expectancy and less Physical Attack. The presence of female rats in mixed colonies would increase the Expectancy. In a situation where there is no artificial manipulation (male colonies) or in which the intervention is small (mixed colonies) correlation between those factors (Physical Attack and Expectancy) is high, that is to say, these factors are close to one another. But when there is a clearer interference, like social isolation, the two factors separate and reveal themselves to be independent from one another. Thereafter, we have analyzed the possible influence of individual differences in a low-frightening Open Field in aggressive behaviour. On the Physical Attack factor the interaction Ambulation-Defecation is nearly significant and the correlations of Ambulation and Defecation with Physical Attack are positive and negative, respectively and nearly significant in mixed colonies but not in isolated rats. We suggest in accordance with Karli, Vergnes, Eclancher, Schmitt and Chaurand (1972) that in an appetite situation the less fearful rats (low defecatory and high ambulatory rats) attack with higher frequency and intensity.     

Mouse aggression and the intruder-familiarity effect: evidence for multiple-factor determination c57bl

Male house mice attack their familiar cagemates less than novel intruders-an effect often attributed to habituation of aggression toward odors emanating from the cagemate. This interpretation is overly simplistic in that the effects of familiarizing preexposure depend additionally upon two factors. One factor is the aggression-inhibiting odors emanating from the test male that are deposited onto the cagemate by cohabitation. Supporting evidence is that attack inhibition to the cagemate failed to generalize to noncohabiting same-strain intruders and that eliminating physical contact between subject and cagemate during preexposure prevented the usual postexposure decline in aggression. The second factor is nonolfactory social stimuli emanating from the cagemate during aggressive encounters. The same intruder odors that elicited aggression when placed on a socially active mouse elicited only investigation when placed on models. When subjects were preexposed to an intruder's odor while prevented from socially interacting with the intruder, this investigation subsequently declined while aggression paradoxically increased.     

The influence of preexperimental experience on social discrimination in rats (Rattus norvegicus)

The authors used laboratory rats (Rattus norvegicus) of known relatedness and contrasting familiarity to assess the potential effect of preexperimental social experience on subsequent social recognition. The authors used the habituation-discrimination technique, which assumes that multiple exposures to a social stimulus (e.g., soiled bedding) ensure a subject discriminates between the habituation stimulus and a novel stimulus when both are introduced simultaneously. The authors observed a strong discrimination if the subjects had different amounts of preexperimental experience with the donors of the 2 stimuli but a weak discrimination if the subjects had either equal amounts of preexperimental experience or no experience with the stimuli. Preexperimental social experience does, therefore, appear to influence decision making in subsequent social discriminations. Implications for recognition and memory research are discussed.     

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.