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Behavioral Reactivity to Social and Nonsocial Stimulations: A Multivariate Analysis of Six Inbred Rat Strains

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Abstract

Male rats from six inbred rat strains (Spontaneously Hypertensive Rat, Wistar Kyoto, Brown Norway, Wistar Furth, Fischer 344, and Lewis) have been compared for their behavioral reactivity when placed in several nonsocial (elevated plus-maze, open field) and social (social interaction in aversive and neutral environment, resident–intruder test, chronic social stress) settings. In addition, a factorial analysis was performed to assess how the variables measured in these different tests related to each other. Besides significant strain-related differences in all tests, the factorial analysis showed that, in nonsocial environments, the strains contrasted essentially along two independent behavioral traits, the propensity to approach or avoid an aversive stimulus and general motor activity in novel environments (two indices of emotionality). In the social settings, marked interstrain differences were observed regarding the expression of aggressive behaviors but these differences were not related to the respective levels on the two nonsocial components of reactivity. Furthermore, large genetic differences were observed in variations of body weight induced by a chronic social stressor paradigm. The factorial analysis suggested a lack of relationship between the effect of social stressors on body weight and the measures of emotionality and general activity obtained in the nonsocial tests. Conversely, these variations were influenced by the levels of aggressiveness and sociability. Taken together, these results show (i) that the behavioral variability observed in rats, in social and nonsocial environments, is influenced by genetic factors and (ii) that the behavioral reactivity to social stimulations is a specific feature, dissociable from the levels of the different components of emotionality (approach/avoidance and general activity) as evaluated by the behavioral responses to nonsocial settings.

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REFERENCES

  • Albonetti, M. E., and Farabollini, F. (1994). Social stress by repeated defeat: Effects on social behavior and emotionality. Behav. Brain. Res. 62:187–193.

    Google Scholar 

  • Benton, D., and Brain, P. F. (1979). Behavioral comparisons of isolated, dominant and subordinate mice. Behav. Process. 4:211–219.

    Google Scholar 

  • Benus, R. F., Den Daas, S., Koolhaas, J. M., and Van Oortmerssen, G. A. (1990). Routine formation and flexibility in social and nonsocial behaviour of aggressive and nonaggressive male mice. Behaviour 112:177–193.

    Google Scholar 

  • Benus, R. F., Bohus, B., Koolhaas, J. M., and Van Oortmerssen, G. A. (1991). Heritable variation for aggression as a reflection of individual coping strategies. Experientia 47:1008–1018.

    Google Scholar 

  • Billingslea, F. Y. (1941). The relationship between emotionality and various other salients of behavior in the rat. J. Comp. Psychol. 31:69–77.

    Google Scholar 

  • Blanchard, R., Hori, K., Tom, P. and Blanchard, D. C. (1988). Social dominance and individual aggressiveness. Aggress. Behav. 14:195–203.

    Google Scholar 

  • Blanchard, C., Spencer, R. L., Weiss, S. M., Blanchard, R. J., McEwen, B., and Sakai, R. R. (1995). Visible burrow system as model of chronic stress: Behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20:117–134

    Google Scholar 

  • Broadhurst, P. L. (1962). A note on further progress in a psychogenetic selection experiment Psychol. Rep. 10:65–66.

    Google Scholar 

  • Castanon, N., and Mormède, P. (1994). Psychobiogenetics: adapted tools for the study of the coupling between behavioral and neuroendocrine traits of reactivity. Psychoneuroendocrinology 19:257–282.

    Google Scholar 

  • Chaouloff, F., Castanon, N., and Mormède, P. (1994). Paradoxical differences in animal models of anxiety among the roman rat lines. Neurosci. Lett. 182:217–221.

    Google Scholar 

  • Comsa, J., Leonardt, H., and Weherle, W. (1982). Hormonal coordination of the immune response. Rev. Physiol. Behav. Pharmacol. 92:115–191.

    Google Scholar 

  • Crunch Software (1991). Crunch Version 4 Statistical Package, Vol. II. Statistics, Crunch Software Corp.

  • Curé, M., and Prolinat, J. P. (1992). Behavioral heterogeneity in Sprague-Dawley rats. Physiol. Behav. 51:771–774.

    Google Scholar 

  • Eleftheriou, B. E., Bailey, D., and Denenberg, V. H. (1974). Genetic analysis of fighting behavior in mice. Physiol. Behav. 13:773–777.

    Google Scholar 

  • Ely, D. L., and Henry, J. P. (1978). Neuroendocrine response patterns in dominant and subordinate mice. Horm. Behav. 10:156–169.

    Google Scholar 

  • Fernandez-Espejo, E., and Mir, D. (1990). Ethological analysis of the male rat's socioagonistic behavior in a resident-intruder paradigm. Aggres. Behav. 16:41–55.

    Google Scholar 

  • File, S. E. (1980). The use of social interaction as method for detecting anxiolytic activity of chlordiazepoxyde-like drugs. J. Neurosci. Methods 2:219–238.

    Google Scholar 

  • File, S. E. (1991). The biological basis of anxiety. In Meltzer H. Y., and Nerozzi, D. (eds.), Current Practices and Future Developments in the Pharmacotherapy of Mental Disorders, Elsevier, Amsterdam, pp. 159–165.

    Google Scholar 

  • Fujita, O., Annen, Y., and Kitaoka, A. (1994). Tsukuba high and low emotional strains of rats: an overview. Behav. Genet. 24:389–415.

    Google Scholar 

  • Garcia-Sevilla, L. (1984). Extraversion and neuroticism in rats. Person. Indiv. Diff. 5:511–532.

    Google Scholar 

  • Gentsch, C. Lichtsteiner, M., and Feer, H. (1991). Genetic and environmental influences on reactive and spontaneous locomotor activities in rats. Experientia 47:998–1007.

    Google Scholar 

  • Goto, S. H., Conceiçao, I. M., Ribeiro, R. A., and Frussa-Filho, R. (1993). Comparison of anxiety measured in the elevated plus-maze, open field and social interaction tests between spontaneously hypertensive rats and Wistar EPM-1 rats. Brazil. J. Med. Biol. Res. 26:965–969.

    Google Scholar 

  • Grant, E. C., and Mackintosh, J. H. (1963). A comparison of the social postures of some common laboratory rodents. Behaviour 21:246–259.

    Google Scholar 

  • Grauer, E., and Kapon, Y. (1993). Wistar Kyoto rats in the Morris water maze: Impaired working memory and hyperreactivity to stress. Behav. Brain Res. 59:147–151.

    Google Scholar 

  • Gray, J. A. (1979). Emotionality in male and female rodents: A reply to Archer. Br. J. Psychol. 70:425–440.

    Google Scholar 

  • Hall, C. S. (1934). Emotional behavior in the rat. I. defecation and urination as measures of individual differences in emotionality. J. Comp. Psychol. 18:385–403.

    Google Scholar 

  • Haller, J., Barna, I., and Baranyi, M. (1995). Hormonal and metabolic responses during psychosocial stimulation in aggressive and nonaggressive rats. Psychoneuroendocrinology 20:65–74.

    Google Scholar 

  • Hendley, E. D., Ohlsson, W. G., and Musty, R. E. (1992). Aggression and hypertension in hypertensive and/or hyperactive rats. Physiol. Behav. 51:1041–1046.

    Google Scholar 

  • Kudryavtseva, N. N., Bakshtanovskaya, I. V., and Koryakina, L. A. (1991). Social model of depression in mice of C57BL/6J strain. Pharmacol. Biochem. Behav. 38:315–320.

    Google Scholar 

  • Lagerspetz, K. M. J. (1964). Studies on the aggressive behavior of mice. Ann. Finn. Acad. Sci. Ser. B 131:1–31.

    Google Scholar 

  • Launay, F., Mills, A. D., and Faure, J. M. (1991). Social motivation in japanese quail chicks selected for high or low levels of treadmill behavior. Behav. Process. 24:95–110.

    Google Scholar 

  • Lemaire, V., and Mormède, P. (1995). Telemetered recording of blood pressure and heart rate in different strains of rats during chronic social stress. Physiol. Behav. 58:1181–1188.

    Google Scholar 

  • McKittrick, C., Blanchard, C. D., and Sakai, R. R. (1995). Serotonin receptor binding in a colony model of chronic social stress Biol. Psychiatry 37:383–393.

    Google Scholar 

  • Mendl, M., Zanella, A. J., and Broom, D. M. (1992). Physiological and reproductive correlates of behavioral strategies in female domestic pigs. Anim. Behav. 44:1107–1121.

    Google Scholar 

  • Mills, A. D., and Faure, J. M. (1991). Divergent selection for duration of tonic immobility and social reinstatement behavior in japanese quail chicks. J. Comp. Psychol. 105:25–38.

    Google Scholar 

  • Mills, A. D., Jones, R. B., and Faure, J. M. (1993). Responses to isolation in Japanese quail genetically selected for high or low sociality. Physiol. Behav. 53:183–189.

    Google Scholar 

  • Mormède, P., Lemaire V., Castanon, N., Dulluc, J., Laval, M., and Le Moal, M. (1990). Multiple neuroendocrine responses to chronic social stress: Interaction between individual characteristics and situational factors. Physiol. Behav. 47:1099–1105.

    Google Scholar 

  • Mos, J., Olivier, B., Poth, M., and Van Aken, H. (1992). The effect of intraventricular administration of eltoprazine, 1-(3-trifluoromethylphenyl) piperazine hypocloride and 8-hydroxy-2-(di-n-propylamino) tetralin on resident-intruder aggression in the rat. Eur. J. Pharmacol. 212:295–298.

    Google Scholar 

  • Ossenkopp, K. P., Sorenson, L., and Mazmanian, D. S. (1994). Factor analysis of open-field behavior in the rat (Rattus novergicus): Application of the three-way PARAFAC model to a longitudinal data set. Behav. Proc. 31:129–144.

    Google Scholar 

  • Paré, W. P., and Redei, E. (1993). Depressive behavior and stress ulcer in Wistar Kyoto rats. J. Physiol. (London) 87:229–238.

    Google Scholar 

  • Popova, N. K., Nikulina, E. M., and Kulikov, A. V. (1993). Genetic analysis of different kinds of aggressive behavior. Behav. Genet. 23:491–497.

    Google Scholar 

  • Potegal, M., and Myers, M. M. (1989). SHR male rats are more aggressive than those of their normotensive progenitor strain. Behav. Neural Biol. 51:247–261.

    Google Scholar 

  • Raab, A., Dantzer, R., Michaud, B., Mormède, P., Taghzouti, K., Simon, H., and Le Moal, M. (1986). Behavioral, physiological and immunological consequences of social status and aggression in chronically coexisting resident-intruder dyads of male rats. Physiol. Behav. 36:223–228.

    Google Scholar 

  • Sapolsky, R. M. (1991). Testicular function, social rank and personality among wild baboons. Psychoneuroendocrinology 16:281–293.

    Google Scholar 

  • Schuurman, T. (1981). Endocrine Processes Underlying Victory and Defeat in the Male Rat, Ph.D. thesis, State University of Groningen, Groningen, The Netherlands.

  • Serova, L. I., and Koslova, L. (1992). Social dominance: Role of genotype and brain epinephrine. In Stress: Neuroendocrine and Molecular Approaches, Gordon and Breach Science, New York, pp. 81–86.

    Google Scholar 

  • Svare, B. B., and Leshner A. I. (1973). Behavioral correlates of intermale aggression and grouping in mice. J. Comp. Physiol. Psychol. 85:203–210.

    Google Scholar 

  • Taylor, G. T., Weiss, J., and Rupich, R. (1987). Male rat behavior, endocrinology, and reproductive physiology in a mixed-sex, socially stressful colony. Physiol. Behav. 39:429–433.

    Google Scholar 

  • Trullas, R., and Skolnick, P. (1993) Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology 111:323–331.

    Google Scholar 

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Correspondence to Olivier Berton.

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Berton, O., Ramos, A., Chaouloff, F. et al. Behavioral Reactivity to Social and Nonsocial Stimulations: A Multivariate Analysis of Six Inbred Rat Strains. Behav Genet 27, 155–166 (1997). https://doi.org/10.1023/A:1025641509809

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  • DOI: https://doi.org/10.1023/A:1025641509809

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