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Social stress induces glucocorticoid resistance in subordinate animals.

Introducing an aggressive intruder into a cage of mice (social disruption, SDR) resulted in intense fighting and defeat of the cage residents. Defeat was accompanied by elevated levels of serum corticosterone and nerve growth factor (NGF). Repeated exposure to an intruder induced a state of glucocorticoid resistance in peripheral immune cells. The present study sought to examine the behavioral factors that mediated the development of glucocorticoid resistance following SDR. Glucocorticoid resistance developed in animals that exhibited a subordinate behavioral profile, which consisted of a low tendency for social investigation and a high level of submissive behavior in response to the intruder's attacks. Glucocorticoid resistance was also linked to the presence of injuries due to fighting, but not to changes in systemic levels of either corticosterone or NGF. Since a submissive behavioral profile is associated with increased risk for injuries due to fighting, it may be that the development of glucocorticoid resistance is an adaptive mechanism that allows the inflammatory component of wound healing to occur in the presence of high levels of corticosterone. Together, these findings demonstrate that the outcomes of social stress may be modified by physiological changes associated with wounding, as well as by behavioral variables such as social status.

Animals↗

Social structure features in three inbred strains of mice, C57Bl/6J, Balb/cj, and NIH: a comparative study.

Some features of social living were investigated in three inbred strains of mice: C57Bl/6j, Balb/cj, and NIH. Five social behaviors--Aggression, Submission, Allogrooming, Social Rest and Rest Alone, as well as Wheel Running Activity--were recorded 2 h daily for a week, in 26 groups of seven male mice living in an enriched environment. Dominants and subordinates among strains shared some behavioral characteristics, but strain contributions upon social structure were also detected. Similarities among strains included the appearance of a single dominant mouse per group rated as the most aggressive, besides from being the animal presented with most Submissions. Allogrooming was more frequent among subordinates than among dominants and subordinates. Differences among strains were that agonistic behavior among subordinates was higher in the Balb/cj and NIH groups than in the C57Bl/6j mice. NIH mice were recorded in Rest Alone more often than mice from the other strains. C57Bl/6j dominants showed higher rates of Wheel Running Activity than subordinates.

Aggression↗

Mechanisms of behavioral switching.

No animal performs only one behavior, so nervous systems must have ways to switch between different behaviors. In this issue of Journal of Comparative Physiology A, several papers discuss how nervous systems achieve this ordered switching between behaviors, from short-term motor control problems, to medium-term decision making based on past experience, to long-term modulation and selection of overall behavioral strategies, such as dominance versus subordinance.

Animals↗

Influence of social dominance on self-stimulation behavior in male golden hamsters.

The effect of a socially dominant hamster on the self-stimulation behavior of the subordinate hamster was examined. After determining social ranking, six hamsters were trained to press a lever in an operant chamber in which a dominant hamster was presented over a grid wall. The threshold of rewarding effect was evaluated by using a descending series of current intensity as electrical reward. When a dominant hamster was present, the subordinate hamster showed a shift of intensity-response function to the right (higher intensity). The presence of a subordinate hamster did not influence the response in dominant hamsters. Furthermore, beta-carboline (FG-7142) (5, 10, and 20 mg/kg, IP) caused a decrease in rewarding effect in dose-dependant manner. These results suggest that the presence of a dominant animal may have caused "a state of anxiety" somewhat similar to the anxiety caused by the benzodiazepine inverse agonist.

Animals↗

Hyperthermic reactions of voles to novel and repetitive psychogenic stimuli.

Montane voles (Microtus montanus) respond to brief conspecific encounters with strange voles by adrenergic reactions which result in elevations of their core temperatures by approximately 1.0 degrees C. Elevations of body temperatures and agonistic behaviors decrease in intensity with sequential encounters between the same conspecific challengers but are restored when one of the challengers is replaced by a new "strange" vole. The rates of habituation of agonistic behaviors and of hyperthermic response are a function of the number of encounters permitted, rather than time between encounters. Levels of hyperthermic responses resulting from contact between previously habituated animals are higher than those elicited by non-specific stimuli such as noise or handling. Radiotelemetry of feral animal temperature homeostasis may provide a useful measure of low-frequency social encounters between conspecific voles.

Animals↗

Expectations of obese trainees: how stigmatized trainee characteristics influence training effectiveness.

This study identifies stigma as a potential precursor to self-fulfilling prophecies in training interactions. Expectations held by leaders often result in actions that elicit expectancy-confirming behaviors from their subordinates. The results of the present study suggest that trainee weight (manipulated with a photograph depicting the trainee as either obese or average weight for height) influenced female trainer expectations and evaluations of the training and trainee. Furthermore, the results suggest that negative expectations held by trainers were related to trainee evaluations of the training and the trainer and, for less flexible trainers, to decrements in trainee performance on the trained task. Overall, the results suggest that trainer expectations can be influenced by stereotypes held about trainee characteristics, thus undermining training effectiveness.

Adult↗

Neurobiological mechanisms of social anxiety disorder.

OBJECTIVE: The authors critically surveyed several preclinical and clinical neurobiological models of social anxiety disorder. METHOD: The authors reviewed the recent literature regarding three animal models of particular relevance to social anxiety. They then examined the recent literature concerning clinical neurobiological aspects of social anxiety disorder, including the developmental neurobiology of anxiety, the genetics of fear and social anxiety, and challenge and imaging studies. RESULTS: The available animal models are useful paradigms for understanding the features of social subordination stress, attachment behavior, and environmental rearing, but they incompletely account for the known neurobiology of human social anxiety disorder. The clinical neurobiology literature surveyed implicates specific neurotransmitter system abnormalities, most notably of the dopamine system, but largely ignores neurodevelopmental processes and the functional interactions between neurotransmitters. Both heritable factors and environmental stress factors appear to be responsible for the onset of social anxiety disorder. CONCLUSIONS: Social anxiety disorder should be conceptualized as a chronic neurodevelopmental illness that might represent a fully compensated state in adulthood. Future investigations from this perspective are discussed.

Adult↗

Managers' tactics of influence: perceptions of regular and temporary employees.

The paper concerns managers' perceived influence tactics with regular and temporary employees. 156 subordinates completed the Behavioral Alteration Techniques Scale. Mean ratings of managers' use of tactics of influence with regular employees were significantly higher than those with temporary employees on 9 of the 22 measured techniques.

Communication↗

Psychosocial stress alters ethanol's effect on open field behaviors.

Psychosocial stress, including social rank status, has been shown to alter spontaneously occurring behaviors in rodents as well as the behavioral effects of drugs of abuse. In this study, rats were repeatedly evaluated in a modified open field following: their initial exposure, and after intraperitoneal injections of saline and 0.75 g/kg ethanol (EtOH). All subjects were first tested while under single housing conditions, then again following 35 days of differential housing (singly or 3 rats/cage) with social status determined by scoring agonistic behavior at triad formation. The data suggest that (1) future subordinate rats differed with respect to specific aspects of behavior displayed in a 'novel' open field arena, (2) future subordinate rats were more emotional since they showed greater "anxiety-like" behavior and less exploratory behavior, (3) subordinate rats were more impaired by the saline injection stress, (4) subordinate rats were more sensitive to the depressant effects of EtOH, (5) grooming behavior did not show habituation, in contrast to the other behaviors, but showed sensitization on the second test. Overall, subordinate rats may have differed from their cage mates in innate anxiety, and this may underlie their distinct response to both stressors and EtOH. Furthermore, while EtOH had mostly stimulant effects in naive rats, psychosocial stress and/or repeated testing resulted in enhancement of EtOH's depressant effects.

Animals↗

6. Social dominance and serotonin receptor genes in crayfish.

Gene expression affects social behavior only through changes in the excitabilities of neural circuits that govern the release of the relevant motor programs. In turn, social behavior affects gene expression only through patterns of sensory stimulation that produce significant activation of relevant portions of the nervous system. In crayfish, social interactions between pairs of animals lead to changes in behavior that mark the formation of a dominance hierarchy. Those changes in behavior result from changes in the excitability of specific neural circuits. In the new subordinate, circuits for offensive behavior become less excitable and those for defensive behavior become more excitable. Serotonin, which is implicated in mechanisms for social dominance in many animals, modulates circuits for escape and avoidance responses in crayfish. The modulatory effects of serotonin on the escape circuits have been found to change with social dominance, becoming excitatory in dominant crayfish and inhibitory in subordinates. These changes in serotonin's effects on escape affect the synaptic response to sensory input of a single cell, the lateral giant (LG) command neuron for escape. Moreover, these changes occur over a 2-week period and for the subordinate are reversible at any time following a reversal of the animal's status. The results have suggested that a persistent change in social status leads to a gradual change in the expression of serotonin receptors to a pattern that is more appropriate for the new status. To test that hypothesis, the expression patterns of crayfish serotonin receptors must be compared in dominant and subordinate animals. Two of potentially five serotonin receptors in crayfish have been cloned, sequenced, and pharmacologically characterized. Measurements of receptor expression in the whole CNS of dominant and subordinate crayfish have produced inconclusive results, probably because each receptor is widespread in the nervous system and is likely to experience opposite expression changes in different areas of the CNS. Both receptors have recently been found in identified neurons that mediate escape responses, and so the next step will be to measure their expression in these identified cells in dominant and subordinate animals.

Animals↗

Behavioral and physiological characterization of male mice under chronic psychosocial stress.

Social stress is a major factor in the etiology of several psychopathologies, with individuals greatly differing in vulnerability. The development of appropriate animal models of social stress is, thus, a major challenge of modern bio-medical research. Adult male mice were subjected to a new model of chronic psychosocial stress in which resident/intruder dyads live chronically in sensory contact and physically interact on a daily basis. Four behavioral categories were identified: Resident Dominants (RD), Resident Subordinates (RS), Intruder Dominants (InD), Intruder Subordinates (InS). Here we investigated: behavior during aggressive interactions; gross physiological components of mice metabolism; organ physiology; response to dexamethasone suppression test (DST). RD and InD mice showed persistently high levels of aggression. All four categories of mice showed robust lack of suppression of corticosterone level when challenged with the DST. Although food intake was not altered under chronic stress, body weight decreased in RD and InD mice while increased in InS and, even more so, in RS mice, suggesting an alteration of their metabolic functions. In conclusion, social status and territory ownership were factors determining individual vulnerability to stress exposure. Our model could, thus, be regarded as a valid model to investigate the biological basis of the individual differences in the response to stressful events.

Aggression↗

[Social rank and depression--an example of "evolutionary psychopathology"].

Affective disorders are pathological alterations of phylogenetically old emotional mechanisms the adaptive function of which is still a matter of debate. According to the social competition hypothesis, depressive syndromes involve activation of a mechanism serving subordination in competitive situations. This mechanism protects the individual from the damaging consequences of an escalating agonistic encounter. The paper critically discusses supporting evidence culled from biological, clinical and psychological findings. Animal models show phenomenological similarities between subordination and depression. In primates affiliative behavior and social bonding are closely linked to rank-related behaviors. Common biochemical and pharmacological features of subordination and depression include an activation of the stress axis, diminished serotonergic neurotransmission and modification by antidepressants. However, the discrimination between a specific subordination reaction and an unspecific stress response is often controversial. Many clinical and psychological aspects of depressive syndromes may be understood as an--exaggerated--submissive behavior, but have rarely been studied in that light. Typical endogenous depression and bipolar disorders challenge the social competition hypothesis. While the manic syndrome, due to its similarity to dominance behavior, supports the link between social competition and affective disorders, the cyclic alteration of mood cannot be sufficiently explained by the social competition hypothesis alone.

Biological Evolution↗

Social stress and corticosterone regionally upregulate limbic N-methyl-D-aspartatereceptor (NR) subunit type NR(2A) and NR(2B) in the lizard Anolis carolinensis.

Social aggression in the lizard Anolis carolinensis produces dominant and subordinate relationships while elevating corticosterone levels and monoaminergic transmitter activity in hippocampus (medial and mediodorsal cortex). Adaptive social behavior for dominant and subordinate male A. carolinensis is learned during aggressive interaction and therefore was hypothesized to involve hippocampus and regulation of N-methyl-d-aspartate (NMDA) receptors. To test the effects of social stress and corticosterone on NMDA receptor subunits (NR), male lizards were either paired or given two injections of corticosterone 1 day apart. Paired males were allowed to form dominant-subordinate relationships and were killed 1 day later. Groups included isolated controls, dominant males, subordinate males and males injected with corticosterone. Brains were processed for glutamate receptor subunit immunohistochemistry and fluorescence was analyzed by image analysis for NR(2A) and NR(2B) in the small and large cell divisions of the medial and mediodorsal cortex. In the small granule cell division there were no significant differences in NR(2A) or NR(2B) immunoreactivity among all groups. In contrast, there was a significant upregulation of NR(2A) and NR(2B) subunits in the large pyramidal cell division in all three experimental groups as compared with controls. The results revealed significantly increased NR(2A) and NR(2B) subunits in behaving animals, whereas animals simply injected with corticosterone showed less of an effect, although they were significantly increased over control. Upregulation of NR(2) subunits occurs during stressful social interactions and is likely to be regulated in part by glucocorticoids. The data also suggest that learning social roles during stressful aggressive interactions may involve NMDA receptor-mediated mechanisms.

Aggression↗

Patterns of neural circuit activation and behavior during dominance hierarchy formation in freely behaving crayfish.

Creation of a dominance hierarchy within a population of animals typically involves a period of agonistic activity in which winning and losing decide relative positions in the hierarchy. Among crayfish, fighting between size-matched animals leads to an abrupt change of behavior as the new subordinate retreats and escapes from the attacks and approaches of the dominant (Issa et al., 1999). We used high-speed videography and electrical recordings of aquarium field potentials to monitor the release of aggressive and defensive behavior, including the activation of neural circuits for four different tail-flip behaviors. We found that the sequence of tail-flip circuit excitation traced the development of their dominance hierarchy. Offensive tail flipping, attacks, and approaches by both animals were followed by a sharp rise in the frequency of nongiant and medial giant escape tail flips and a fall in the frequency of offensive tail flips of the new subordinate. These changes suggest that sudden, coordinated changes in the excitability of a set of neural circuits in one animal produce the changes in behavior that mark its transition to subordinate status.

Action Potentials↗

Social environment determines the long-term effects of social defeat.

A single social defeat by a dominant conspecific induces long-term changes in several physiological and behavioral parameters in rats. These changes may represent an increased vulnerability to subsequent stress and stress-related pathology. Environmental factors, in particular possibilities for social interactions, could modulate these effects. Therefore, we assessed the influence of social environment on susceptibility for the long-term effects of social defeat. Socially housed males of an unselected strain of wild-type rats were equipped with radio-telemetry transmitters that recorded heart rate, temperature and activity. They were individually subjected to defeat and subsequently either housed alone or returned to their group. Behavioral and physiological responses to various novelty stressors were determined during a three-week period after the social defeat. Furthermore, changes in baseline behavior and physiology following defeat were studied in the rat's homecage. The results show a complex interaction between defeat and housing conditions. Depending on the parameters measured, effects were caused by both isolation alone, defeat alone or a combination of both defeat and isolation. Individual housing alone caused a characteristic hyperactive response to novelty stress. Though defeat did not affect behavioral responses, it amplified the physiological response to novelty and social housing did not attenuate this effect. However, social housing did reduce the effects of defeat on heart rate, temperature and activity in the home cage and completely prevented defeat-induced weight loss. Together these results indicate that social housing may indeed positively affect the animal's capacity to cope with stressors.

Analysis of Variance↗

Similarity of 5-HT2 receptor sites in dominant and subordinate vervet monkeys.

Pharmacological studies using serotonergic agents have revealed status-linked behavioral effects in dominant and subordinate vervet monkeys. A possible explanation for the greater drug response observed in dominant animals is that there is a CNS difference between dominant and subordinate animals. Such differences could exist at the level of serotonin receptor sites, membrane responsiveness, or interaction with other neurotransmitters. We have examined the specific 3H-ketanserin binding in various regions of vervet monkey brain to evaluate the hypothesis that dominant and subordinate vervet monkeys differ in CNS 5-HT2 receptor sites. No differences were found in the number or affinity of 3H-ketanserin binding sites between dominant and subordinate animals. Further, no differences were found in the displacement of 3H-ketanserin binding by the serotonin agonist quipazine. These results suggest the conclusion that differences at 5-HT2 binding sites do not account for status-linked differences in behavioral drug response in vervet monkeys and that other or additional mechanisms must underlie status-related drug response differences.

Animals↗

Effects of alcohol on aggressive behavior in squirrel monkeys: influence of testosterone and social context.

Social status and reproductive cycle determine the effects of acute, low doses of alcohol on the social behavior of squirrel monkeys. Alcohol produces biphasic effects on the behavior of dominant but not subordinate monkeys, and only during the mating season. The change in alcohol sensitivity measured in dominant monkeys coincides with changes in plasma testosterone levels. In order to directly study the interaction between alcohol, testosterone and aggressive behavior, testosterone propionate (TP, 25 mg/kg/day, SC) was administered to either dominant or subordinate male monkeys belonging to four separate groups, resulting in significantly elevated plasma levels of testosterone (i.e., 905 +/- 43 ng/ml in subordinates; 171 +/- 19 ng/ml in dominants). Two to three weeks after the beginning of testosterone treatment, the monkeys were administered doses of alcohol (0.1-1.0 g/kg). The behavior of subordinate monkeys was unaffected by TP treatment (even after the dominant monkey from each colony was removed and housed separately for 6 weeks). Testosterone treatment altered the sensitivity of subordinate monkeys to alcohol. Low doses of alcohol increased the frequency of threats, grasps, and displacements exhibited by subordinate monkeys with exogenously elevated testosterone. Daily administration of TP to dominant monkeys during the non-mating season did not affect the behavior of the treated animals in the group, although the body weight of TP-treated monkeys was similar to that measured during the mating season. Low doses of alcohol increased the frequency of threats, grasps, and displacements in dominant monkeys maintained on TP. We also tested the role of social context in maintaining high levels of plasma testosterone, and alcohol sensitivity in dominant monkeys.(ABSTRACT TRUNCATED AT 250 WORDS)

Aggression↗