Aggression is suppressed by acute stress but induced by chronic stress: Immobilization effects on aggression, hormones, and cortical 5-HT1B/ striatal dopamine D2 receptor density

Although it has been established by a number of investigators that a variety of stressors are associated with the induction of aggressive behavior, two specific issues remain unanswered. First, it is unclear whether the contexts surrounding stressors (e.g., stressor length and chance of winning over opponents) change outcomes regarding aggressive behavior. Second, if a relationship exists between stress and aggressive behavior, altered levels of stress-related hormone (e.g., corticosterone [CORT]), as well as aggression-related biomarkers (e.g., testosterone [T], density of prefronto-cortical 5-HT(1B) receptor and striatal dopamine D(2) receptor [D2r]) may contribute to changes in aggressive behavior. Thus, we examined how immobilization (with a 1-, 5-, or 10-day exposure) would impact (1) a longitudinal course of aggression toward different-sized opponents, (2) levels of CORT and T, and (3) densities of 5-HT(1B) receptor (5-HT1Br) in the prefrontal cortex (PFC) and D2r in the striatum. It was found that, regardless of small or large opponents, a single 2-h exposure to immobilization reduced aggressive behavior (stress-suppressed aggression) over time, whereas repeated (10-day) exposure to immobilization escalated aggressive behavior (stress-induced aggression). These stress effects persisted up to 1 week of recovery from immobilization stress. Moreover, immobilized rats demonstrated elevated levels of T, but not CORT, as compared with controls. Finally, acute immobilization altered D2r densities in the shell of the nucleus accumbens, and chronic immobilization changed 5-HT1Br in the PFC, including the downregulation of 5-HT1Br densities in the right prelimbic and orbitolateral cortices. The potential relationships among stress, aggression, and 5-HT1Br/D2r roles are discussed.     

Cardiovascular and testosterone responses to contested dominance in women

Examined cardiovascular and testosterone responses of dominant and submissive women to an acute stressor involving contested dominance. Twenty (10 dominant, 10 submissive) university students rated their dominance to a predefined reference group, participated in a task that involved debating with a trained technician, and were continuously provided with bogus feedback throughout the task concerning biochemical substances in their blood that purportedly covaried with dominance. Covariance analyses revealed that dominant women were much more reactive to the stressor in several cardiovascular parameters than those classified as submissive. Serum testosterone did not vary as a function of the experimental manipulation, and at each measurement point, dominant and submissive subjects had essentially identical serum levels of this hormone. Interestingly, however, baseline testosterone for the dominant group was related to changes in systolic blood pressure (i.e., gain scores computed as task response minus baseline values).     

The influence of an audience upon the reactions to filmed violence

In order to examine audience effects when viewing firmed violence, 5 to 6 year old pre-school boys who had been rated as submissive by their teachers watched an aggressive or a neutral movie either alone, accompanied by another submissive classmate, or a dominant one. Subsequent aggression against a frustrating, unknown and unseen boy was delivered via a modified Buss machine, especially adapted for children. Subjects accompanied by a dominant peer were more aggressive than the others but did not react differentially to the movies. Subjects tested alone were more aggressive after the violent film than after the neutral one and the opposite pattern occurred for the boys accompanied by a submissive classmate. These findings stress the importance of the social context when viewing filmed violence. It is suggested that the quality of the audience can have different directional (e.g. fear and aggression) as well as energizing properties. Links with the literature on social facilitation and audience effects are underlined.     

Grooming expresses harderian gland materials in the blind mole rat

The blind mole rat (Spalax ehrenbergi) is a highly aggressive and solitary rodent that shows the most striking physiological and behavioral adaptations to underground life. The eyes are not detectable externally; they are atrophied and covered by a thick layer of skin. A considerable part of the orbit is occupied by a very large Harderian gland. The current study demonstrates that during autogrooming the mole rat expresses Harderian gland materials from the conjunctival sac to the external nares and spreads them onto the fur. In contrast to other rodents, the mole rat's grooming behavior is usually confined to the front part of the body and does not progress after the head wipes to ventrolateral torso licking. Moreover, in highly aggressive encounters grooming sometimes ceases after the second phase-the nose wipe bouts. The unique first phase of the mole rat's grooming consists of highly rapid strokes over the skinny border of the head, which we assume help to squeeze Harderian materials from the gland. Unlike other rodents, in which grooming occupies a considerable part of their waking time, mole rats, cage individually, rarely perform autogrooming behavior. Grooming in mole rats has been found to be highly correlated with aggressive encounters, and submissive animals exhibit significantly more grooming than their dominant opponents. It is speculated that the Harderian gland discharge may serve as an appeasing substance when mole rats meet to reduce the extreme aggressiveness typical of these subterranean rodents. © 1995 Wiley-Liss, Inc.     

Acute stress persistently enhances estrogen levels in the female rat

Here we tested whether exposure to either tailshock or swim stress alters ovarian hormone levels, estrogen and progesterone, in females and whether the effects are persistent. Adrenal hormone levels were also measured in males and females. Estradiol levels were elevated in unstressed females during proestrus relative to females in other stages of estrous, and exposure to the stressors enhanced estradiol beyond basal levels. For females stressed during diestrus 2, estradiol levels were elevated immediately after stressor cessation and up to 24 hrs. Exposure to tailshock, but not swim-stress, transiently enhanced progesterone in females stressed during the stage of proestrus and estrus. Glucocorticoid levels were elevated in response to both stressors and were supraelevated in females under both basal and stress conditions relative to males, particularly in blood from females exposed to acute swim stress. These results indicate that exposure to a relatively acute stressful event immediately and persistently enhances serum estradiol and are discussed in the context of reports that exposure to the same stressors immediately and persistently impairs associative learning in the female rat.     

Permanent and transient effects of repeated preweaning stress on social and sexual behaviors of rats

We have reported that exposure of preweaning male and female rats to a model of unpredictable mild physical stressors (Neo-A) can decrease the behavioral and hormonal responses to acute and chronic stress as adults. In this paper we have analyzed the effect of Neo-A on development of social behaviors, including aggressiveness, social dominance, and sexual behavior in adulthood. The subjects were divided into two groups: Neo-A (daily exposed to unpredictable mild stresses- from day 2 up to day 15 of suckling; n = 30 litters) and controls (C) (undisturbed rats, except for testing, during the same period of life; n = 26 litters). When day 6 pups were submitted to a social clustering test the Neo-A group showed a higher rate of litter-mate clustering than C. The 35 days Neo-A males and Neo-A females submitted to a social behavior test after 24 h of social isolation also showed higher scores of time spent in active social interaction than controls, as well as a higher ratio of animals showing aggressive playing. A second social behavior test performed after 48 h of social isolation at days 75-80 of age revealed that only Neo-A females displayed increased social behavior and aggressive behaviors, whereas controls did not. A water competition test performed at 24 and 48 h after water deprivation showed that Neo-A adult males spent more time in possession of the drinking device and drank more frequently than C. When adult proestrous females were exposed to a sexual behavior test, the Neo-A group showed shorter latency and higher scores of lordosis quotient. These results support the view that exposure to this model of repeated mild stress early in life stimulates the development of social behavior, dominance and sexual behavior.     

Social dominance and individual aggressiveness

Male rats exhibiting high, moderate, or low levels of offensive aggressive behavior in interactions with intruders in their home cage were grouped in mixed-sex colonies with 1 male of each aggression-level group in each colony. Agonistic interactions measured 1, 2, 3, 7, 14, 21, and 22 days after colony formation indicated that highly aggressive males on pretests continued to be more aggressive, becoming the dominant colony male in five of seven colonies and attacking intruders more often than less aggressive males. In the two remaining colonies the moderately aggressive male became dominant. This relationship, which was consistent over a number of indices, including offensive and defensive behaviors, and wound counts and wound sites, was seen even when a substantial weight differential favored the less aggressive animal. Dominance relationships were rapidly established and within-group fighting declined significantly over the 21-day test period. Pretest offensive levels also influenced the behavior of subordinates, with high or moderately aggressive subordinates showing more defense in interactions with dominants and receiving more wounds than did low-aggression subordinates. Dominant males also showed more defense in interacting with those subordinates which had been more aggressive during pretests. This pattern of results suggests that aggression level of the subordinate as well as the dominant may be an important factor determining the intensity of agonistic interactions in male rats.     

Effect of neonatal handling on adult rat spatial learning and memory following acute stress

Brief neonatal handling permanently alters hypothalamic-pituitary-adrenal axis function resulting in increased ability to cope with stress. Since stress is known to affect cognitive abilities, in the present study we investigated the effect of brief (15 min) handling on learning and memory in the Morris water maze, following exposure to an acute restraint stress either before training or recall. Exposure of non-handled rats to the acute stress prior to training resulted in quicker learning of the task, than in the absence of the stressor. When acute stress preceded acquisition, male handled rats showed an overall better learning performance, and both sexes of handled animals were less impaired in the subsequent memory trial, compared to the respective non-handled. In addition, the number of neurons immunoreactive for GR was higher in all areas of Ammon's horn of the handled rats during the recall. In contrast, the number of neurons immunoreactive for MR was higher in the CA1 and CA2 areas of the non-handled males. When the acute restraint stress was applied prior to the memory test, neonatal handling was not effective in preventing mnemonic impairment, as all animal groups showed a similar deficit in recall. In this case, no difference between handled and non-handled rats was observed in the number of GR positive neurons in the CA2 and CA3 hippocampal areas during the memory test. These results indicate that early experience interacts with sex and acute stress exposure in adulthood to affect performance in the water maze. Hippocampal corticosterone receptors may play a role in determining the final outcome.     

Short- and long-term effects of juvenile stressor exposure on the expression of GABAA receptor subunits in rats

During the juvenile period rodents are particularly sensitive to stressors. Aversive events encountered during this period may have enduring effects that are not evident among animals initially stressed as adults. Interestingly, experiencing stressor during juvenile period was found to elicit a biphasic behavioral pattern over the course of development. During the juvenile period, the expression of several GABAA receptor subunits is subject to elevated plasticity, rendering the GABAergic system sensitive to stressors. In the present investigation, animals were exposed to a juvenile variable stressor regimen (JUV-S) at 27-29 postnatal days (PND): 27 PND-acute swim stress (10 min), 28 PND-elevated platform stress (3 sessions×30 min each), and 29 PND-restraint (2 h). One hour following the last exposure to stressor or in adulthood (60 PND), anxiety-related behaviors were assessed in a 5-min elevated plus maze test. The western blotting technique was used to evaluate whether the juvenile stress induced behavioral pattern will be accompanied by respective changes in GABAA α1, α2, and α3 protein expression in male rats. Our findings further established that juvenile stressor elicits hyper-reactivity when rats were tested as juveniles, whereas rats exhibited reduced activity and increased anxiety when tested as adults. Additionally, the effects of juvenile stressor on α1, α2, and α3 were more pronounced among juvenile stressed rats that were challenged as adults compared with rats that were only challenged as juveniles. Interestingly, the stress-induced modulation of the subunits was particularly evident in the amygdala, a brain region closely associated with anxiety. Thus, age- and region-specific alterations of the α subunits may contribute to the age-specific behavioral alterations observed following juvenile stress exposure.     

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.     

Working memory performance after acute exposure to the cold pressor stress in healthy volunteers

Effects of acute stress exposure on learning and memory have been frequently studied in both animals and humans. However, only a few studies have focused specifically on working memory performance and the available data are equivocal. The present study examined working memory performance during the Sternberg item recognition task after exposure to a predominantly adrenergic stressor. Twenty four healthy subjects were randomly assigned to a stress group or a control group. The stress group was exposed to the cold pressor stress test (CPS; i.e. insertion of the dominant hand into ice water for 60s), while 37 °C warm water was used with the control group. Twenty minutes after the stress exposure, working memory performance was tested with the Sternberg item recognition task with three levels of cognitive load. Sympathetic nervous system and hypothalamic pituitary adrenocortical (HPA) axis activation during CPS, were assessed by measuring heart rate and salivary cortisol before and during (heart rate) or 30 min after (cortisol) the stress procedure. Exposure to the CPS test was associated with a significant increase in heart rate but no increase in salivary cortisol. Participants exposed to the stress procedure showed significantly shorter reaction times during trials with higher cognitive load but tended to show higher false alarm rates than control subjects. The present results indicate that exposure to CPS can be associated with signs of both enhanced and impaired working memory performance. The observed behavioral pattern might represent a form of streamlined information processing advantageous in a threatening situation.     

Stress exposure and affective modulation of aggressive behavior in men and women

To study differences in the effects of stress exposure and affective responding on aggression in men and women, the authors examined the effects of an acute stressor (air blast) on subsequent aggressive behavior, measured as the intensity of shocks men and women delivered to a putative employee. The authors measured participants' affective responding using the startle reflex. Results showed that although men and women did not differ in their startle responses to the actual stressor, high stress led to contrasting patterns of subsequent aggressive behavior. Women under high stress responded with less aggression than women under low stress, whereas men exposed to high stress exhibited increases in aggression relative to those under low stress. Affective responding during the stressor differentially modulated aggression in men and women: Startle responses predicted increasing levels of aggression in men and less aggression in women. These findings suggest that although men and women show similar basic affective processing in response to stressors, the behavioral profiles associated with stress differ in men and women. These findings have implications for understanding gender differences in the prevalence of internalizing and externalizing psychopathology.     

Effects of repetitive stress during the acute phase of Trypanosoma cruzi infection on chronic Chagas' disease in rats

The effect of repetitive stress during acute infection with Trypanosoma cruzi (T. cruzi) on the chronic phase of ensuing Chagas' disease was the focus of this investigation. The aim of this study was to evaluate in Wistar rats the influence of repetitive stress during the acute phase of infection (7 days) with the Y strain of T. cruzi on the chronic phase of the infection (at 180 days). Exposure to ether vapor for 1 min twice a day was used as a stressor. Repetitive stress enhanced the number of circulating parasites and cardiac tissue disorganization, from a moderate to a severe diffuse mononuclear inflammatory process and the presence of amastigote burden in the cardiac fibers. Immunological parameters revealed that repetitive stress triggered a reduced concanavalin A induced splenocyte proliferation in vitro with major effects on the late chronic phase. Serum interleukin-12 concentration decreased in both stressed and infected rats in the early phase of infection although it was higher on 180 days post-infection. These results suggest that repetitive stress can markedly impair the host's immune system and enhance the pathological process during the chronic phase of Chagas' disease.     

Influence of dominance on the development of play fighting in pairs of male Syrian golden hamsters (Mesocricetus auratus)

In the highly social rat, male juvenile and adult subordinates initiate more playful contacts with dominant pairmates than vice versa. This study examined the effect of dominance on playful contacts in the relatively asocial golden hamster. Pairs of male hamsters were reared together from weaning, and their play was filmed in the juvenile (28-36 days) and the young adult (60-70 days) stages of development. By the adult stage, it became clear that one pairmate was dominant over the other. The dominant pairmate launched all aggressive attacks (i. e., bites to the lower flanks and rump), and the subordinate pairmate performed all the submissive gesturing (e. g., tail up submissive posture). Playful contact, which in this species involves gentle nibbling of the posterior cheeks, was more frequently launched by the dominant than by the subordinate. This was not only true at the adult stage, but also at the juvenile stage, before dominance-subordination relationships were sharply polarized. Therefore, it would appear that in the relatively asocial hamster, the subordinates tend to avoid playful contact with dominants. This is markedly different to rats, where the subordinates actively seek out and engage dominants in play. This contrast further supports our hypothesis that subordinate male rats use play as a means of maintaining familiarity with dominants. © 1993 Wiley-Liss, Inc.     

Male aggression in the presence of an estrous female.

The relationship between male rat aggressiveness and the presence of a female was studied. Twenty 100-day-old dominant male albino rats were individually exposed to an inaccessible female rat in a specially constructed apparatus. The males were then given free-forced trials to an empty compartment or a compartment housing a submissive male. The results indicate that following exposure to an estrous female, dominant males increased their percentage of choices to the submissive male. Moreover, the incidences of aggressions by the dominant animal toward the submissive animal increased sharply after prior exposure to the estrous female. These data suggest that one antecedent source of aggression among male rodents may be the presence of a sexually receptive female.     

In Vivo Hippocampal Acetylcholine Release During Exposure to Acute Stress

Hippocampal extracellular acetylcholine (ACh) and choline levels were evaluated using in vivo microdialysis in male Fischer 344 rats before, during, and following an 80-min exposure to two different stress conditions. Measurements were taken in rats restrained and immersed in a water bath containing either 37 degreesC (normothermic-restraint) or 20 degreesC (cold-restraint) water. Results were compared to normothermic-freely-moving rats. Cold-restrained rats displayed decreased ACh levels during cold exposure relative to both normothermic-restrained and normothermic-freely-moving rats. By the end of the cold exposure period and following removal from cold, ACh levels had returned to near-baseline values. Normothermic-restrained rats had levels similar to those of normothermic-freely-moving rats, except for a marked increase in ACh following removal from restraint. Cold-restrained rats displayed a gradual elevation in choline levels during cold stress, followed by a gradual decline after stress termination, whereas both normothermic-restrained and normothermic-freely-moving rats displayed gradual decreases during the microdialysis session. These findings demonstrate that central cholinergic neurotransmission can be altered by the application of, and removal from, acute stressors. In addition, the results suggest a possible relationship between the magnitudes of both the stressor and its cholinergic consequences.     

Acute stress impairs trace eye blink conditioning in females without altering the unconditioned response

Exposure to an acute stressor of inescapable swimming or intermittent tail shocks impairs classical eye blink conditioning 24h later in female rats. This effect is often attributed to a deficit in "learning," but since stress has been shown to induce analgesia, an alternative explanation is that stressor exposure reduces conditioning by lessening the perceived intensity of the unconditioned stimulus (US). To address this possibility we examined the amplitude of the unconditioned response (UR) during training and found that although exposure to the stressor impaired trace conditioning, there was no difference in the UR amplitude. We also found that eye blink responses to different US intensities (4-12 V) in the absence of training were unaffected by stressor exposure. Taken together, these experiments indicate that the stress-induced impairment of conditioning in females is not due to a decreased perception of US strength.     

Oral concentration of volatile sulphur compounds in stressed rats

Stress has been identified as a halitosis-inducing factor. Halitosis may be measured by the determination of oral volatile sulphur compound levels (VSC). Since immobilization and swimming are two experimental protocols widely used to induce stress in laboratory animals, the aim of this work was to investigate the influence of stress on VSC in rats. Male Wistar rats were submitted to three swimming or immobilization sessions over consecutive days. The oral VSC increased 3 h after the first and third swimming or immobilization sessions. The results in the present study support the hypothesis that stress may be an etiological factor in halitosis. Also, the animal experimental design may represent a new approach to research concerning the relationship between halitosis and stress.     

The noradrenergic system and its involvement in aggressive behaviors

Although a multitude of variables are associated with the expression of aggression, it is imperative that accurate neurochemical vulnerabilities be understood. Norepinephrine is one neurochemical that has been linked to aggressive behavior displayed by nonhuman and human animals. The purpose of the present review was to interpret research findings regarding this relationship. The authors evaluated previous research in order to determine whether a reliable connection between norepinephrine and aggressive behavior exists. Moreover, the potential nature of the norepinephrine–aggressive behavior relationship is presented. In general, research has found a positive relationship between levels of norepinephrine and aggressive behavior among nonhuman animals and humans. However, multiple studies reporting contradictory results were also reviewed that suggest a nonlinear relationship. Norepinephrine's relationship with aggressive behavior may best be explained in terms of the stress–response system and the type of aggressive behavior elicited. Limitations of the previous studies and ideas for future research are discussed.     

Contextual influences on interpersonal complementarity

The influence of context on interpersonal complementarity was examined using an event-contingent recording procedure. Setting and role status moderated the relation between how a person behaved and how the other person behaved. Individuals were more likely to respond with agreeable behavior to agreeableness in others when not at work than when at work and when in a high status work role relative to a low status work role. Reciprocity between dominance and submissiveness was found in work settings but not in nonwork settings. Individuals were more likely to reciprocate more submissive behavior by the other person with more dominant behavior and more likely to reciprocate more dominant behavior by the other person with relatively more submissive behavior when in a higher status work role relative to lower status work roles. Results were interpreted in terms of the influence of decreased structure and shared goals on increasing interpersonal complementarity.