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S-3.-Social aggression in animals: acute and long-term effects on behavior and physiology

Koolhaas, Jaap M.
Department of Animal Physiology, University of Groningen, Haren, The Netherlands

Sgoifo, Andrea
Dipartimento di Biologia Evolutiva e Funzionale, Università di Parma, Parma, Italy.

Symposium Abstract

In social species, most individuals face a certain level of stress deriving from aggressive interactions with conspecifics. Some of them, by achieving a sufficient degree of control over their social environment, may cope well whereas others, uncapable of adopting adequate coping strategies, may suffer and develop various symptoms of stress-related pathology. Today, there is a considerable amount of experimental work describing in detail the effects of social stressors on physiology and behavior. The aim of this symposium is to call together a number of scientists which, despite belonging to different scientific disciplines (neurobiology, psychoneuroendocrinology, psychiatry, cardiovascular physiology, ethology) share an interest for the behavioral and physiological consequences of social aggression in animal models. The symposium will illustrate which consequences negative social stimuli may have on neuroendocrine systems, on cardiovascular function, on circadian rhythms, on social and sexual behavior. It will also provide provide some examples which could help in answering the question: “What can experimental studies on social stress in animals tell us about stress-related disorders in humans and which implications do such studies have for clinical practice ?

S-3.1.-Intermittent social conflict: acute and long-term autonomic consequences in  rats

Sgoifo, A., Meerlo*, P., Pozzato, C.,  Manghi, M.,  Stilli, D., Musso, E. and Koolhaas**, J. M.
Dipartimento di Biologia Evolutiva e Funzionale, Università di Parma, Parma, Italy
* Department of Neurobiology and Physiology,  Northwestern University, Evanston,  IL-USA
** Dept. Animal Physiology, University of Groningen, Haren, The Netherlands

In rats, social conflicts produce acute autonomic and neuroendocrine effects as well as long-lasting changes of circadian rhythms of heart rate, body temperature and physical activity. This paper describes the impact of dominant-subordinate as compared to dominant-dominant aggressive confrontations on: 1) autonomic balance and susceptibility to cardiac arrhythmias during stress exposures, and 2) daily rhythms of heart rate (HR), temperature (T), and physical activity (Act) following social conflicts. Wild-type males (6-month-old, n=12) were instrumented with telemetry ECG/Temperature/Activity transmitters and confronted in their own territory for 10 consecutive times with a young male which they sistematically attacked and submitted (dominant-subordinate interactions, DSI). Six days after the last victory, each animal was introduced in the territory of another dominant male, resulting in fierce fighting (dominant-dominant interaction, DDI). ECGs were recorded in baseline, test and recovery periods (15-min each) during 1st and 10th DSI and in DDI. Rhythms of HR, T, and Act were monitored before and after each social challenge. Although all the three stressors produced significant reductions of average RR interval, such decrements were significantly larger in DDI than in the two DSIs. In addition, RR variability (expressed as SDRR, SD/RR and r-MSSD) was significantly reduced in DDI, whereas it was unchanged in both DSIs. These data suggest that in dominant rats confronted with same rank males the sympathovagal balance is shifted toward a sympathetic dominance, whereas it is substantially maintained when they are confronted with a subordinate male. Consistent with this finding is the incidence of ventricular premature beats, which was significantly larger in DDI as compared to both DSIs. DSIs did not produce any effect on the daily rhythms of HR, T, and Act. In contrast, DDI resulted in a significant decrease in the daily amplitude of the rhythms, which lasted for two weeks. The individual changes in rhythm amplitude did not correlate with the  number of attacks received from the territory owner; on the contrary, they negatively correlated with the aggression exhibited by the experimental rats themselves (number of counter-attacks). Therefore, the long-term consequences of a social conflict in rat do not seem to depend on the physical intensity of the fight in terms of aggression received, rather on the subjects coping strategy.

S-3.2.-Behavioral and physiological consequences of chronic subordination stress.

Blanchard, D.C.
Pacific Biomedical Research Center and Department of Genetics and Molecular Biology, John A. Burns School of Medicine, University of Hawaii at Manoa. Honolulu, Hawaii, USA

Behavioral and endocrine consequences of chronic subordination stress have been demonstrated in a wide range of mammalian species and in nonmammalian vertebrates as well.  Behavioral components include enhanced defensiveness, reduced activity, exploration, and appetitively motivated behavior; variations in sleep-waking cycles; and increased voluntary consumption of psychoactive drugs. Regional brain neurotransmitter system differences of subordinates compared to controls or dominants have been shown for a variety of monoamines; for amino acids; and for neuropeptides. Endocrine consequences of chronic social stress include high magnitude changes in both central and peripheral regulation of adrenal and gonadal steroids. These differences for chronically socially stressed subordinates provide parallels to the behavioral and physiological changes associated with some stress-linked psychopathologies.

S-3.3.-Effect of repeated social stress on c-fos expression in the rat brain.

Martinez, M., Calvo-Torrent, A., Valverde-Navarro*, A.A., Picó-Alfonso, M.A., Payá-Cano, J.L., Martinez-Soriano, F. and  Herbert**, J.
Area of Psychobiology, Faculty of Psychology, University of Valencia, Spain;
*Department of Morphological Sciences, Faculty of Medicine, University of Valencia;
**Department of Anatomy, MRC Cambridge Centre for Brain Repair, University of Cambridge, UK. 

Defeat resulting from intraspecific encounters between male rats represents a biologically relevant form of social stress. In order to assess the changes induced in the neural activity in animals exposed to defeat, immediate early gene (e.g. c-fos) expression is used. The objective of this study was to determine the pattern of adaptation of the neural activity when animals are exposed repeatedly to defeat. To this purpose, Lister hooded male rats were exposed to the attack of a larger male along 1, 2, 5, 10, or 20 consecutive days in the latter's home cage. Control animals were exposed to an empty cage. C-fos expression (quantified using image analysis) in the forebrain and brainstem sixty minutes after the last defeat was analyzed. The results obtained indicate that acute defeat induced an increase of neural activity in most of the brain areas studied in comparison with control animals. However, when animals were exposed to repeated defeat during different periods of time, the pattern of adaptation was highly regionally specific. In some areas, such as the lateral septum, the central and cortical amygdala, the lateral hypothalamic area, and the lateral and medial divisions of the paraventricular nucleus the hypothalamus, c-fos expression decreased with increasing exposure to defeat. However, in other areas, such as the prefrontal cortex, the raphe nuclei and central grey, this decrease was not observed. Differently, other areas such as the bed nucleus of the stria terminalis, the medial amygdala, the dorsal division of the paraventricular nucleus and the locus ceruleus firstly showed a decrease in the activity but later increased again. In conclusion, the present study shows that the brain adapts to repeated social defeat in a specific manner. Furthermore, studying animals over comparatively prolonged periods may yield a more complete picture of the dynamics of the neural response to chronic social stress. Implications of the changes in neural response to the adaptation in other stress responses needs further research. This study was supported by the University of Valencia (n° 2212) and the BBV Foundation.

S-3.4.-Effects of aggressive harassment on male copulatory behavior in Japanese macaques

Troisi, A. and Carosi*, M.
Department of Psychiatry, University of Tor Vergata, Rome, Italy
* Laboratory of Comparative Ethology, NIHCD Animal Center, Poolesville, USA

Disruption of rivals’ mating activity is a prominent strategy for intrasexual competition in many mammal species. The aim of the present study was to analyze the effects of aggressive harassment on different behavioral measures of male copulatory behavior in Japanese macaques (Macaca fuscata). The subjects of the study were adult monkeys living in a stable social group of 82 individuals. During 238 hours of observation, 240 copulations were recorded involving 68 different heterosexual pairs formed by 16 males and 26 females. Data collection method was a combination of “focal group” and “complete record” techniques. A total of 62 episodes of aggressive harassment of consort pairs were recorded. The intensity of harassment displayed by the aggressors ranged from stare threat to physical attack. The frequency of aggressive harassment did not vary with the dominance rank of the consort partners (F=0.41, df=3,65, NS). To assess the impact of aggressive harassment on male copulatory behavior, we correlated the frequency of aggressive harassment with a number of different measures reflecting the efficiency of male sexual performance. The number of episodes of aggressive harassment suffered by each male correlated not only with the number of copulations interrupted before ejaculation because of overt interference (r=0.61, N=16, P<0.005) but also with the number of copulations interrupted before ejaculation without any apparent reason (r=0.81, P<0.0001). In contrast, the frequency of aggressive harassment did not correlate with the total number of ejaculations (r=0.30, NS), the number of different females with whom each male was observed to ejaculate (r=0.31, NS), and the mean ejaculation latency (r=0.22, NS). To explain these conflicting results, we hypothesize that, in a multi-male group living in a large enclosure with several visual barriers, high-ranking males have much difficulty trying to reduce rivals’ global mating success through aggression, even though aggressive harassment disrupts a consistent percentage of rivals' mount series.

S-3.5.-Single social defeat in rats: temporal dynamics of the stress response.

Koolhaas, J.M., Buwalda,  B., Ruis,  M.A.W. and de Boer, S.F.
Department of Animal Physiology, University of Groningen,  Haren, The Netherlands.

A single social defeat in male rats has long-term physiological and behavioral consequences. Depending on the parameter, changes may last from several hours up to days and weeks. This makes the model highly suitable for the study of the processes in time underlying the development of affective disorders. Highly characteristic for affective disorders in human beings is the reduction in 5-HT neurotransmission and the changes in the HPA axis. Pharmacological challenge tests, using serotonergic agonists demonstrate a gradually developing diminished corticosterone and hypothermia response. Initially a hyperreactivity of ACTH and corticosterone to a CRH challenge is observed. At the same time, a gradual reduction of the corticosterone feedback develops, as reflected by an enhanced ACTH and corticosterone response in the dexamethasone CRH challenge test. This is accompanied by changes in MR and GR binding having a different course in time in different brain areas. Hence, HPA axis regulation changes gradually at various levels of organisation. Despite these changes in regulation, plasma levels of corticosterone remain relatively constant after the defeat. The dynamic changes in behavior and physiology depend on the social housing conditions after the defeat. It seems that the absence of social support after the social defeat is essential for the development of depression-like symptoms in the male rat. The temporal dynamic of the various stress parameters implies that the state of the animal shortly after the stressor will be different from the state several days or weeks later, i.e. the syndrome depends on the time of measurement after the stress experience. Therefore, it is often misleading to label these symptoms as signs of human psychopathology. In fact, the social defeat model allows a detailed analysis of the cascade of events triggered by a traumatic live event. Understanding this cascade in terms of causal and sequential processes and the conditions that might speed up or delay its progressive character is relevant in understanding the etiology of human affective disorders.