Aggressive behavior in female hamsters: the hormonal basis for fluctuations in female aggressiveness correlated with estrous state

The frequency and sequencing of aggressive behaviors by naive female hamsters change during series of brief encounters, probably because of the lack of stable dominance relations. Such initial encounters seem most representative of interactions likely in free-ranging hamsters and have been emphasized in studies of the hormonal mediation of female aggression. Nonestrous females exhibit intense aggression toward conspecifics of either sex. Estrous females are not aggressive and spend much time in lordosis, indicative of sexual receptivity. The inhibition of fighting on estrous day depends on estrogen and progesterone. Whereas oil-injected adrenalectomized-ovariectomized females fight at high levels, comparable with intact nonestrous females, the combination of 17 beta-estradiol benzoate and progeterone suppresses fighting completely. In contrast, replacement of estradiol, progesterone, or testosterone propionate individually has on consistent effect. Hypophysectomized females also fight at high levels, indicating that pituitary hormones are not required for vigorous aggression. Further, individual anterior pituitary hormones did not produce marked changes in fighting. These results emphasize the roles of estrogen and progesterone in synchronizing aggression with current reproductive state.     

Immune stress in late pregnant rats decreases length of gestation and fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring

Immune challenge during pregnancy is associated with preterm birth and poor perinatal development. The mechanisms of these effects are not known. 5α-Pregnan-3α-ol-20-one (3α,5α-THP), the neuroactive metabolite of progesterone, is critical for neurodevelopment and stress responses, and can influence cognition and affective behaviours. To develop an immune challenge model of preterm birth, pregnant Long-Evans rat dams were administered lipopolysaccharide [LPS; 30?μg/kg/ml, intraperitoneal (IP)], interleukin-1β (IL-1β; 1?μg/rat, IP) or vehicle (0.9% saline, IP) daily on gestational days 17-21. Compared to control treatment, prenatal LPS or IL-1β reduced gestational length and the number of viable pups born. At 28-30 days of age, male and female offspring of mothers exposed to prenatal IL-1β had reduced cognitive performance in the object recognition task compared to controls. In females, but not males, prenatal IL-1β reduced anxiety-like behaviour, indicated by entries to the centre of an open field. In the hippocampus, progesterone turnover to its 5α-reduced metabolites was lower in prenatally exposed IL-1β female, but not in male offspring. IL-1β-exposed males and females had reduced oestradiol content in hippocampus, medial prefrontal cortex and diencephalon compared to controls. Thus, immune stress during late pregnancy reduced gestational length and negatively impacted birth outcomes, hippocampal function and central neurosteroid formation in the offspring.     

An exploratory study on self‐evaluated aggression and androgens in women

Healthy, premenopausal women completed the Buss‐Perry Aggression Questionnaire. Venous blood samples were taken at the mid‐cycle phase of the menstrual cycle to determine plasma androgen levels. Total and free testosterone, 5α‐dihydrotestosterone, androstenedione, and dehydroepiandrosterone were assessed. Path analyses were aimed at finding out which of the five circulating hormones might best predict a latent aggression construct derived from the four subscales of the Aggression Questionnaire. A significant correlation was found between free testosterone and physical and verbal aggression subscales. In addition, the results demonstrate for the first time in women a significant link between 5α‐dihydrotestosterone and anger. Thus, both testosterone and 5α‐dihydrotestosterone may affect, by separate pathways, the basal regulation of aggression‐proneness in women. Aggr. Behav. 28:273–280, 2002. © 2002 Wiley‐Liss, Inc.     

Prelordotic behavior in the hamster: a hormonally modulated transition from aggression to sexual receptivity

The behavioral responses of the female golden hamster to a sexually experienced male were analyzed as a function of the stage of the female's estrous cycle. Exogenous estradiol or estradiol followed by progesterone was given to ovariectomized females to determine the role of these hormones in the regulation of cyclic changes in the female's response to the male. Females were paired on a daily basis with sexually active males for 10 min, and behavioral interactions were recorded. Significantly more fighting occurred during early diestrus than later in the cycle. During the 24 hr preceding sexual receptivity, fighting was infrequent. BY 8 HR PRIOR TO THE ONSET OF SEXUAL RECEPTIVITY, 86% OF THE POPULATION EXHIBITED A BEHAVIOR RESEMBLING THE ONSET OF LORDOSIS WITHOUT IMMOBILIZATION (PRELORDOSIS). Following ovariectomy fighting was at a high level (80%--90%). Estradiol replacement, over a 28-day test period, resulted in a significant decrease in aggression and a significant increase in the display of the prelordotic response without inducing lordosis. Initially, the treatment with progesterone following 7 days of estradiol treatment caused the female to display lordosis. After 24 hr a significant increase in aggression, which continued as long as progesterone was present, was observed. After removal of progesterone a significant decrease in aggression occurred. Thus, estradiol causes the female to become tolerant of the male's approach, the female exhibiting prelordosis in response to the male's investigation. Estradiol and progesterone are necessary for normal sexual receptivity; however, after 24 hr, estrogen-progesterone-treated females become agonistic to the male.     

Urinary testosterone metabolite levels and aggressive behaviors in male and female bonobos (Pan paniscus)

This study presents the first data on the relationship between testosterone (T) and aggression in both sexes of the bonobo (Pan paniscus). Morning urinary concentrations of T metabolites (measured by immunoreactive 5α–androstane–17α–ol–3–one) were used to reflect T status. Results show that first, no correlation of T metabolite levels with any of the aggressive behaviors was found between individuals. Within an individual, T metabolite levels only correlated with a minority of aggressive behaviors. Hence, social factors are likely of major importance for the occurrence of aggression in this highly gregarious species, but certain intraindividual aspects of aggressive behavior are nevertheless related to T. A more detailed discussion of the results follows. Secondly, all correlations with T were similar for every individual, males and females, suggesting an analogous relationship in both sexes. Thirdly, our study confirms for bonobos that the measure of aggression used, the time scale at which the correlation is studied, and whether this is done on an inter‐ or intraindividual level, considerably affect results. Aggr. Behav. 30:425–434, 2004. © 2004 Wiley‐Liss, Inc.     

Juvenile offspring of rats exposed to restraint stress in late gestation have impaired cognitive performance and dysregulated progestogen formation

Gestational stress may have lasting effects on the physical and neurocognitive development of offspring. The mechanisms that may underlie these effects are of interest. Progesterone and its 5α-reduced metabolites, dihydroprogesterone and 5α-pregnan-3α-ol-20-one (3α,5α-THP), maintain pregnancy, have neurotrophic effects, and can enhance cognitive performance. We hypothesized that some of the deleterious effects of gestational stress on the cognitive performance of offspring may be related to progestogen formation. Pregnant rat dams were exposed to restraint under a bright light (thrice daily for 45 min) on gestational days 17-21 or were minimally handled controls. Dams that were exposed to restraint had lower circulating levels of 3α,5α-THP and significantly greater concentrations of corticosterone at the time of birth than did control dams. Male and female offspring, that were gestationally stressed or not, were cross-fostered to non-manipulated dams. Between postnatal days 28-30, offspring were assessed for object recognition, a prefrontal cortex (PFC)-dependent cognitive task. Restraint-exposed offspring performed more poorly in the object recognition task than did control offspring, irrespective of sex. As well, progesterone turnover to its 5α-reduced metabolites in the medial PFC (but not the diencephalon) was significantly reduced among restraint-exposed, compared to control, offspring. Progesterone turnover, and levels of 3α,5α-THP, positively correlated with performance in the object recognition task. Thus, restraint stress in late pregnancy impaired cognitive development and dysregulated progestogen formation in brain.     

Prenatal testosterone treatment potentiates the aggression‐inhibiting effect of the neurosteroid dehydroepiandrosterone in female mice

The neurosteroid dehydroepiandrosterone (DHEA) is a powerful inhibitor of aggression in murine models when given for 15 days and potentially may be useful in the management of inappropriate human aggression. Although the biosynthesis and metabolism of DHEA have been described, little is known about the potential effect of the steroidal environment during sexual differentiation on the subsequent response to DHEA. Whether prenatal androgen exposure influences the subsequent response to DHEA was assessed by comparing the effect of DHEA (80 μg/d) on aggression in female offspring where dams were treated with 1, 10, or 100 μg of testosterone (T) on days 15 to 18 of gestation (Experiment I) or that developed in different uterine positions (Experiment II). The results showed that DHEA decreased attack behavior in general and that the 100‐μg prenatal T treatments enhanced the antiaggressive effect of this neurosteroid. Neither the lower doses of exogenously administered T nor the uterine position led to an enhanced response to DHEA. In addition, whether DHEA produced changes in social and nonsocial activities was examined. In the 100‐μg T females, DHEA increased the duration of the former and decreased the frequency and duration of the latter, indicating that it was not a general decrement in behavioral expression that mediated the enhanced response to the antiaggressive effect of DHEA. In the second experiment, DHEA treatment led to increased frequencies of social nonaggressive and nonsocial activities. However, the uterine positions × treatment interactions were not significant, demonstrating that contiguity to male fetuses did not differentially affect the response to DHEA. Aggr. Behav. 27:130–138, 2001. © 2001 Wiley‐Liss, Inc.     

Effect of conspecific sex on aggression during pregnancy and lactation in golden hamsters

The effect of conspecific sex on maternal aggression in hamsters was determined by comparing the frequency of aggressive responses by dams continuously housed with either a virgin male or female cagemate during pregnancy and lactation. Dams easily established aggressive dominance over male cagemates soon after pairing, and their aggression was low thereafter for the duration of pregnancy and lactation. The aggression of dams with females, on the other hand, tended to fluctuate with highs during mid pregnancy and mid lactation and lows around birth. When dam aggression was low around birth, female cagemates frequently became aggressively dominant, and several dams lost their litters. The higher aggression of dams toward females than males is probably a reflection of greater intrasexual competition for environmental resources that includes pups.     

Syrian hamster males below an age threshold do not elicit aggression from unfamiliar adult males

In many species, young males are the dispersers, leaving their natal area after weaning to establish a breeding area of their own. As young males disperse, however, they are bound to encounter unfamiliar adult males with established territories. Such interactions between an adult male and a young male may always be agonistic. Alternatively, there may be an age threshold below which aggression is not elicited and above which the adult male is aggressive toward the juvenile male. To test these two alternative hypotheses, we paired 47 young Syrian hamster (Mesocricetus auratus) males ranging from 24 to 65 days of age with 47 adult male hamsters and measured aggressive and investigatory behavior for 5 min. We observed no aggression by the adult toward young males between 24 and 47 days of age or toward the single male that was 49 days of age. Young males that were 50 days of age or older, however, elicited significant levels of aggression from the adults. These results indicate that in Syrian hamsters, young males are less vulnerable to adult aggression up to an age threshold and are more vulnerable to adult aggression beyond that threshold. This pattern may facilitate the establishment of territories by dispersing young males below that age threshold. Aggr. Behav. 37:91–97, 2011. © 2010 Wiley‐Liss, Inc.     

Intraspecific aggression in male hamsters is inhibited by intrahypothalamic vasopressin-receptor antagonist

The present study examines the effect of the arginine vasopressin (AVP) receptor antagonist, d(CH₂)₅Tyr(Me)AVP, on intraspecific aggression between pairs of male Golden hamsters in a neutral territory. Subjects drawn from a group of 24 animals were paired once each with novel partners from the group under each of three experimental conditions: 1) both members of a pair were microinjected into the anterior hypothalamus with saline (S/S), 2) one member of a pair was microinjected with AVP-receptor antagonist and its partner with saline (A/S), and 3) both members of a pair were microinjected with AVP-receptor antagonist (A/A). There were significantly (P < .01) fewer attacks during encounters between pairs of hamsters in the A/A condition compared to pairs in the A/S condition. Similarly, pairs in the A/S condition attacked significantly (P < .025) less often than pairs of hamsters in the S/S condition. These results confirm our earlier work showing that AVP-receptor antagonist reduces intraspecific aggression. In addition, saline-treated hamsters initiated significantly (P < .001) fewer attacks toward antagonist treated hamsters than would have been predicted if their opponent was not drug treated. These latter results suggest that hamsters microinjected into the anterior hypothalamus with an AVP-receptor antagonist also elicit less aggression from conspecifics.     

Overt and covert aggression in work settings in relation to the subjective well‐being of employees

Aggressive behavior was studied in workplaces having (1) predominantly male, (2) predominantly female, or (3) both male and female employees in equal or near equal frequencies. In addition to examining the occurrence of different types of aggression in these workplaces, the question of whether being a target of aggression is related to employees’ subjective well‐being was addressed. One hundred sixty‐nine participants (mainly 30–50 years of age) employed in a wide range of organizations in the public sector completed a questionnaire measuring four types of observed and experienced aggression: direct overt, indirect manipulative, covert insinuative, and rational‐appearing aggression. Indirect manipulative and rational‐appearing aggression were perceived to be the most widely used aggression styles in the work context. In the predominantly male workplaces, the men were perceived to use more of all types of aggression than in the predominantly female workplaces. The women’s aggression was not related to the relative number of females and males with whom they worked. Participants were divided into two groups on the basis of the extent to which they estimated themselves to be targets of workplace aggression. Those who considered themselves to be victims of workplace aggression suffered significantly more from psychosocial problems and physical symptoms than those who had been victimized to a lesser extent or not at all. The victimized group also considered the aggression they had suffered to be the reason for their psychosocial and health problems. Aggr. Behav. 27:360–371, 2001. © 2001 Wiley‐Liss, Inc.     

Distinguishing among nondirect forms of aggression

This study explored the relationships and differences among two measures of indirect aggression [Bjorkqvist et al., 1994; Richardson and Green, 1997] and one of relational aggression [Crick and Grotpeter, 1995]. Over 300 students (mean age 22.8 years; 61.5% female) from two colleges in the Southeastern United States completed measures of indirect and relational aggression and related constructs (e.g., empathy, anger expression, direct aggression). Although there were subtle differences among the three measures with regard to their relationships with associated variables, overall the patterns of relationships were similar as well as distinct from the pattern for direct aggression. Factor analysis of scores for measures of aggression revealed that the indirect and relational measures composed a single factor of nondirect aggression, separate from direct aggression. Further factor analysis of all unique items from the nondirect scales found the overall construct of nondirect aggression to comprise six distinct factors. Implications for applications and further research are discussed.     

Estrogen Improves Performance of Reinforced T-Maze Alternation and Prevents the Amnestic Effects of Scopolamine Administered Systemically or Intrahippocampally

In a previous study, administration of high doses of estradiol benzoate (100 μg/kg for 3 days im) to ovariectomized Long-Evans rats counteracted impairments of reinforced T-maze alternation induced by systemic administration of scopolamine, a muscarinic receptor blocker. In the current study, daily administration of lower doses of estradiol benzoate (5 μg/kg for 3 weeks sc) increased the number of correct reinforced alternations during T-maze acquisition in ovariectomized rats compared to oil-treated controls and prevented impairments of reinforced alternation induced by injection of scopolamine hydrobromide (0.2 mg/kg ip). Furthermore, scopolamine (20 μg) delivered bilaterally to the dorsal hippocampus reduced reinforced T-maze alternation in ovariectomized rats previously trained to complete this task while daily treatment with estradiol benzoate (5 μg/kg sc) for 1 week prior to scopolamine infusion counteracted this impairment. In summary, physiological levels of estrogen improved performance during acquisition of reinforced T-maze alternation and prevented impairments induced by scopolamine administered systemically or intrahippocampally.     

Reactive aggression tracks within‐participant changes in women's salivary testosterone

The relation between testosterone and aggression has been relatively well documented in men, but it is less well understood in women. Here we assessed the relationship between salivary testosterone and reactive aggression (i.e., rejection rate for unfair offers) in the Ultimatum Game. Forty naturally cycling women were tested twice, once in the late follicular phase (around ovulation) and once during the luteal phase. Ovulation was determined using urine test strips measuring luteinizing hormone levels. Salivary samples were assayed for testosterone, estradiol, progesterone, and cortisol at both test sessions. There was no association with the cycle, but multilevel modeling revealed a significant within‐participant association between testosterone and rejection rate for extremely unfair offers (i.e., high reactive aggression), indicating that women showed greater reactive aggression when their testosterone levels were higher. Additionally, we found that women with relatively high individual concentrations of testosterone were more likely to reject extremely unfair offers than women with relatively low concentrations of testosterone. This study is the first to demonstrate that women react more aggressively in response to provocation when their testosterone level is high than when their testosterone is low, suggesting that testosterone plays an important role in the regulation of women's aggressive behavior following social provocation.

     

Sex differences in genetic and environmental effects on aggression

The aim of the present study was to investigate the genetic and environmental factors influencing teacher and parental rated aggression in boys and girls, asking whether the magnitude of these effects is similar across rater and sex. The study is part of an ongoing nationwide twin‐family study of behavioral development and health habits carried out in Finland. The sample consisted of 1651 twin pairs (264 monozygotic male, 300 monozygotic female, 292 dizygotic male, 278 dizygotic female, and 517 dizygotic opposite‐sex twin pairs), representing subsets of five 11‐ to 12‐year‐old twin cohorts (b. 1983–1987). The data were collected using the teacher and parental rating forms of the Multidimensional Peer Nomination Inventory. Structural equation models of sex‐limitation assessed sex differences in genetic and environmental influences on aggression. The results suggested significant genetic, common environmental, and specific environmental effects on aggression in both boys and girls, but the best fitting model differed depending on the informant. For both ratings, boys showed lower levels of heritability and higher levels of common environment than girls. In addition, the teacher rating data also suggested the presence of either sex‐specific common environmental effects or sex‐specific genetic effects. Support is provided also for sibling contrast effects, either at the behavioral level or as a rater bias. Aggr. Behav. 29:55–68, 2003. © 2003 Wiley‐Liss, Inc.     

Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats

Learning and memory processes may be influenced by fluctuations in steroid hormones, such as estrogens and progestins. In this study, we have used an animal model to investigate the effects of endogenous fluctuations in ovarian steroids in intact female rats and effects of administration of ovarian steroids to ovariectomized rats for non-spatial, working memory using the object recognition task. Performance in this task relies on cortical and hippocampal function. As such, serum, cortical, and hippocampal concentrations of estradiol (E2), progesterone (P4), and P4's metabolite, 5alpha-pregnan-3alpha-ol-20-one (3alpha,5alpha-THP), were measured by radioimmunoassay. Experiment 1: Rats in behavioral estrus, compared to those in diestrus or estrus, spent a greater percentage of time exploring a novel object concomitant with increases in serum E2, P4, and 3alpha,5alpha-THP levels. Regression analyses revealed that there was a significant positive relationship between E2 levels in the hippocampus and 3alpha,5alpha-THP levels in the hippocampus and cortex and performance in this task. Experiment 2: Administration of E2 and/or P4 immediately post-training increased the percentage of time spent exploring the novel object and produced levels of E2, P4, and 3alpha,5alpha-THP akin to that of rats in behavioral estrus. Experiment 3: Post-training administration of selective estrogen receptor modulators, including 17beta-E2, propyl pyrazole triol, and diarylpropionitrile increased the percentage of time spent exploring the novel object compared to vehicle-administration. Experiment 4: Post-training P4 or 3alpha,5alpha-THP administration, compared to vehicle, increased the percentage of time spent exploring the novel object and produced P4 and/or 3alpha,5alpha-THP levels within the physiological range typically observed for rats in behavioral estrus. Experiment 5: If post-training administration of E2 and/or P4 was delayed one hour, no enhancement in object recognition was observed. Together, these results suggest that E2 and progestins can have mnemonic effects through actions in the cortex and/or hippocampus.     

Relational aggression in college students: Examining the roles of social anxiety and empathy

This study examined the unique contributions of social anxiety and empathy to relational aggression in 300 19–to–25–year–old (M=21.25; SD=1.32) male (n=97) and female (n=203) college students using hierarchical linear regression analysis. The interactive relations between gender and social anxiety, and between gender and empathy, were also assessed. In addition to the gender and overt aggression covariates, fear of negative evaluation and perspective taking were unique predictors of relational aggression. Males, students who were more overtly aggressive, and those who reported greater fear of negative evaluation were more relationally aggressive than were peers. Students with higher levels of perspective taking reported using less relational aggression than did peers. A gender x empathetic concern interaction indicated that for males only, lower levels of empathetic concern were associated with higher levels of relational aggression. Results are discussed within a social information‐processing perspective. Aggr. Behav. 29:430–439, 2003. © 2003 Wiley‐Liss, Inc.     

Hormones and competitive aggression in women

This study used diaries of competitive interactions to explore the relationship between hormones and competitive aggression in women. Thirty women completed approximately 10 diary entries each. In each entry, the women described a recent competitive interaction they had engaged in and noted whether it was expressed aggressively or through other tactics. Each woman received a score for the fraction of her competitive interactions that were expressed using physical aggression, verbal aggression, nothing overt, and so on. Hormones (total testosterone, free testosterone, androstenedione, estradiol, and cortisol) were measured in serum early in the follicular phase. Results indicate that women with low levels of androstenedione and total testosterone were less likely to express their competitive feelings overtly, while women with high levels of androstenedione were more likely than other women to express their competitive feelings through verbal aggression. Estradiol was unrelated to competitive tactics, but women with high estradiol levels reported fewer competitive interactions over athletics than did other women. Aggr. Behav. 29:107–115, 2003. © 2003 Wiley‐Liss, Inc.