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Behavior Genetics

, Volume 33, Issue 5, pp 563–574 | Cite as

Toward an Animal Model for Antisocial Behavior: Parallels Between Mice and Humans

  • Frans Sluyter
  • Louise Arseneault
  • Terrie E. Moffitt
  • Alexa H. Veenema
  • Sietse de Boer
  • Jaap M. Koolhaas
Article

Abstract

The goal of this article is to examine whether mouse lines genetically selected for short and long attack latencies are good animal models for antisocial behavior in humans. To this end, we compared male Short and Long Attack Latency mice (SAL and LAL, respectively) with the extremes of the Dunedin Multidisciplinary Health and Development Study (men who persistently displayed antisocial behavior [Persisters] and men who never manifested antisocial behavior [Abstainers]). Groups were compared on the basis of five distinct domains: aggression/violence, reproduction, cognition, behavioral disorders, and endophenotypes. Our observations point to considerable parallels between, on one side, SAL and Persisters, and, on the other side, between LAL and Abstainers (but to a lesser extent). We believe that SAL and LAL are good mouse models to study the development of antisocial behavior and will yield valuable and testable hypotheses with regard to the neurobiological and genetical architecture of antisocial behavior.

Mouse model aggression violence antisocial behavior 

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References

  1. Almasy, L., and Blangero, J. (2001). Endophenotypes as quantitative risk factors for psychiatric disease: Rationale and study design. Am. J. Med. Genet. 105:42-44.Google Scholar
  2. Arseneault, L., Moffitt, T. E., Caspi, A., Taylor, A., Rijsdijk, F., Jaffee, S., Ablow, J. C., and Measelle, J. R. (2003). Strong genetic effects on cross-situational antisocial behavior among 5-year-old children, according to mothers, teachers, examinerobservers, and twin's self-reports. J. Child Psychol. Psychiatry (in press).Google Scholar
  3. Bartels, M., de Geus, E. J., Sluyter, F., Kirschbaum, C., and Boomsma, D. I. (2003a). Heritability of daytime cortisol levels in children. Behav. Genet. (in press).Google Scholar
  4. Bartels, M., van den Berg, M., Sluyter, F., Boomsma, D. I., and de Geus, E. J. (2003b). Heritability of cortisol levels: Review and simultaneous analysis of twin studies. Psychoneuroendocrinology 28:21-37.Google Scholar
  5. Benus, R. F., den Daas, S., Koolhaas, J. M., and van Oortmerssen, G. A. (1990). Routine formation and flexibility in social and non-social behaviour of aggressive and non-aggressive mice. Behaviour 112:176-193.Google Scholar
  6. 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 47:1008-1019.Google Scholar
  7. Bohus, B., Benus, R. F., Fokkema, D. F., Koolhaas, J. M., Nyakas, C., van Oortmerssen, G. A., Prins, A. J. A., De Ruiter, A. J. H., Scheurink, A. J. W., and Steffens, A. B. (1987). Neuroendocrine states and behavioral physiological stress responses. In E. R. de Kloet, V. M. Wiegant, and D. de Wied (Eds.), Progress in brain research, (Vol. 72); pp. 57-70. Amsterdam: Elsevier.Google Scholar
  8. Brodkin, E. S., Goforth, S. A., Keene, A. H., Fossella, J. A., and Silver, L. M. (2002). Identification of quantitative trait loci that affect aggressive behavior in mice. J. Neurosci. 22:1165-1170.Google Scholar
  9. Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H., and van Oost, B. A. (1993). Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262:578-580.Google Scholar
  10. Cadoret, R. J., Yates, W. R., Troughton, E., Woodworth, G., and Stewart, M. A. S. (1995). Genetic-environmental interaction in the genesis of aggressivity and conduct disorders. Arch. Gen. Psych. 52:916-924.Google Scholar
  11. Canastar, A., and Maxson, S. C. (2003). Sexual aggression in mice: Effects of male strain and of female estrous State. Behav. Genet. (this issue). Author please supply missing informationGoogle Scholar
  12. Cases, O., Seif, I., Grimsby, J., Gaspar, P., Chen, K., Pournin, S., Muller, U., Aguet, M., Babinet, C., Shih, J. C. et al. (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 270:1763-1766.Google Scholar
  13. Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., and Craig, I. W. (2002). Role of genotype in the cycle of violence in maltreated children. Science 297:851-854.Google Scholar
  14. Catlett, R. H. (1961). An evaluation of methods for measuring fighting behaviour with special reference to Mus musculus. Anim. Behav. 9:8-10.Google Scholar
  15. Compaan, J. C., Hutchison, J. B., Wozniak, A., de Ruiter, A. J. H., and Koolhaas, J. M. (1994). Brain aromatase activity and plasma testosterone levels are elevated in aggressive male mice during early ontogeny. Brain Res. Dev. Brain Res. 82:185-192.Google Scholar
  16. Compaan, J. C., van Wattum, G., de Ruiter, A. J. H., van Oortmerssen, G. A., Koolhaas, J. M., and Bohus, B. (1993). Genetic differences in female house mice in aggressive response to sex steroid hormone treatment. Physiol. Behav. 54:899-902.Google Scholar
  17. Coward, P., Nagi, K., Chen, D., Thomas, D. H., Nagamine, C., and Lau, Y.-F. C. (1994). Polymorphism of a CAG trinucleotide repeat within Sry correlates with B6.Y*DOM sex reversal. Nat. Genet. 6:245-250.Google Scholar
  18. Crabbe, J. C., Phillips, T. J., Feller, D. J., Hen, R., Wenger, C. D., Lessov, C. N., and Schafer, G. L. (1996). Elevated alcohol consumption in null mutant mice lacking 5-HT1B serotonin receptors. Nat. Genet. 14:98-101.Google Scholar
  19. Crusio, W. E., Schwegler, H., and Lipp, H.-P. (1987). Radial-maze performance and structural variation of the hippocampus in mice: A correlation with mossy fibre distribution. Brain Res. 425:182-185.Google Scholar
  20. de Boer, S. F., van der Vegt, B. J., and Koolhaas, J. M. (2003). Individual variation in aggression of feral rodent strains: A standard for the genetics of aggression and violence? Behav. Genet. (this issue). Author please supply missing informationGoogle Scholar
  21. de Geus, E. J. (2002). Introducing genetic psychophysiology. Biol. Psychol. 61:1-10.Google Scholar
  22. de Geus, E. J., and Boomsma, D. I. (2001). A genetic neuroscience approach to cognition. Eur. Psychologist 6:241-253.Google Scholar
  23. de Ruiter, A. J. H., Koolhaas, J. M., Keijser, J., van Oortmerssen, G. A. and Bohus, B. (1992). Differential testosterone secretory capacity of the testes of aggressive and non-aggressive house mice during ontogeny. Aggress. Behav. 18:149-157.Google Scholar
  24. D'Souza, U. M., Kel, A., and Sluyter, F. (2003). From transcriptional regulation to aggressive behavior. Behav. Genet. (this issue). Author please supply missing informationGoogle Scholar
  25. Eley, T. C., Lichtenstein, P., and Moffitt, T. E. (2003). A longitudinal analysis of the etiology of aggressive and non-aggressive antisocial behaviour. Dev. Psychopathol. (in press).Google Scholar
  26. Fehr, C., Grintschuk, N., Szegedi, A., Anghelescu, I., Klawe, C., Singer, P., Hiemke, C., and Dahmen, N. (2000). The HTR1B 861G>C receptor polymorphism among patients suffering from alcoholism, major depression, anxiety disorders and narcolepsy. Psychiatr. Genet. 10:59-65.Google Scholar
  27. Feldker, D. E., Datson, N. A., Veenema, A. H., Meulmeester, E., de Kloet, E. R., and Vreugdenhil, E. (2003a). Serial analysis of gene expression predicts structural differences in hippocampus of long attack latency and short attack latency mice. Eur. J. Neurosci. 17:379-387.Google Scholar
  28. Feldker, D. E., de Kloet, E. R., Kruk, M. R., and Datson, N. A. (2003b). Large scale gene expression profiling of discrete brain regions. Behav. Genet. (this issue). Author please supply missing informationGoogle Scholar
  29. Gayan, J., Smith, S. D., Cherny, S. S., Cardon, L. R., Fulker, D. W., Brower, A. W., Olson, R. K., Pennington, B. F., and DeFries, J. C. (1999). Quantitative-trait locus for specific language and reading deficits on chromosome 6p. Am. J. Hum. Genet. 64:157-164.Google Scholar
  30. Green, S. (1983). Animal models in schizophrenia research. In G. C. L. Davey (Ed.), Models of human behavior (pp. 315-338). New York: John Wiley & Sons.Google Scholar
  31. Guénet, J. L., and Bonhomme, F. (2003). Wild mice: An everincreasing contribution to a popular mammalian model. Trends Genet. 19:24-31.Google Scholar
  32. Guillot, P.-V., Roubertoux, P. L., and Crusio, W. E. (1994). Hippocampal mossy fiber distributions and intermale aggression in seven inbred mouse strains. Brain Res. 660:167-169.Google Scholar
  33. Hallikainen, T., Saito, T., Lachman, H. M., Volavka, J., Pohjalainen, T., Ryynanen, O. P., Kauhanen, J., Syvalahti, E., Hietala, J., and Tiihonen, J. (1999). Association between low activity serotonin transporter promoter genotype and early onset alcoholism with habitual impulsive violent behavior. Mol. Psychiatry 4:385-388.Google Scholar
  34. Henry, J. P., and Stephens, P. M. (1977). Stress, health and the social environment: A sociobiological approach to medicine. Berlin: Springer Verlag.Google Scholar
  35. Hensbroek, R. A., Sluyter, F., and van Oortmerssen, G. A. (1996). Stress induced free-choice alcohol consumption in aggressive and non-aggressive male mice. Behav. Genet. 26:187.Google Scholar
  36. Hill, E. M., Stoltenberg, S. F., Bullard, K. H., Li, S., Zucker, R. A., and Burmeister, M. (2002). Antisocial alcoholism and serotoninrelated polymorphisms: Association tests. Psychiatr. Genet. 12:143-153.Google Scholar
  37. Hogg, S., Hof, M., Würbel, H., Steimer, T., de Ruiter, A. J. H., Koolhaas, J. M., and Sluyter, F. (2002). Behavioral profiles of genetically selected aggressive and non-aggressive male wild house mice in two anxiety tests. Behav. Genet. 30:439-446.Google Scholar
  38. Holmes, A., Murphy, D. L., and Crawley, J. N. (2002). Reduced aggression in mice lacking the serotonin transporter. Psychopharmacology 161:l60-167.Google Scholar
  39. Jaffee, S. R., Caspi, A., Moffitt, T. E., Taylor, A., and Dickson, N. (2001). Predicting early fatherhood and whether young fathers live with their children: Prospective findings and policy reconsiderations. J. Child Psychol. Psych. 42:803-815.Google Scholar
  40. Jaffee, S., Caspi, A., Moffitt, T. E., Dodge, K., Rutter, M., Taylor, A., and Tully, L. (2003). Genetic vulnerabilities interact with child maltreatment to promote conduct problems (submitted).Google Scholar
  41. Jeglum-Bartusch, D., Lynam, D., Moffitt, T. E., and Silva, P. A. (1997). Is age important: Testing general versus developmental theories of antisocial behavior: Criminology 35:13-47.Google Scholar
  42. Koolhaas, J. M., Korte, S. M., de Boer, S. F., van der Vegt., B. J., van Reenen, C. G., Hopster, H., de Jong, I. C., Ruis, M. A., and Blokhuis, H. J. (1999). Coping styles in animals: Current status in behavior and stress-physiology. Neurosci. Biobehav. Rev. 23:925-936.Google Scholar
  43. Korte, S. M., Meijer, O. C., de Kloet, E. R., Buwalda, B., Keijser, J., Sluyter, F., van Oortmerssen, G. A., and Bohus, B. (1996). Enhanced 5-HT1A receptor expression in forebrain regions of aggressive house mice. Brain Res. 736:338-343.Google Scholar
  44. Kranzler, H., Lappalainen, J., Nellisery, M., and Gelernter, J. (2002). Association study of alcoholism subtypes with a functional promoter polymorphism in the serotonin transporter protein gene. Alcohol Clin. Exp. Res. 26:1330-1335.Google Scholar
  45. Lahr, G., Maxson, S. C., Mayer, A., Just, W., Pilgrim, C., and Reisert, I. (1995). Transcription of the Y chromosomal gene, Sry, in adult mouse brain. Mol. Brain Res. 33:179-182.Google Scholar
  46. Lappalainen, J., Long, J. C., Eggert, M., Ozaki, N., Robin, R. W., Brown, G. L., Naukkarinen, H., Virkkunen, M., Linnoila, M., and Goldman, D. (1998). Linkage of antisocial alcoholism to the serotonin 5-HT1B receptor gene in 2 populations. Arch. Gen. Psychiatry 55:989-994.Google Scholar
  47. Lyons, M. J., True, W. R., Eisen, S. A., Goldberg, J., Meyer, J. M., Faraone, S. V., Eaves, L. J., and Tsuang, M. T. (1995). Differential heritability of adult and juvenile antisocial traits. Arch. Gen. Psych. 53:906-915.Google Scholar
  48. Manuck, S. B., Flory, J. D., Ferrell, R. E., Dent, K. M., Mann, J. J., and Muldoon, M. F. (1999). Aggression and anger-related traits associated with a polymorphism of the tryptophan hydroxylase gene. Biol. Psychiatry 45:603-614.Google Scholar
  49. Manuck, S. B., Flory, J. D., Ferrell, R. E., Mann, J. J., and Muldoon, M. F. (2000). A regulatory polymorphism of the monoamine oxidase-A gene may be associated with variability in aggression, impulsivity, and central nervous system serotonergic responsivity. Psychiatry Res. 95:9-23.Google Scholar
  50. Maxson, S. C. (1996). Search for candidate genes with effects on an antagonistic behavior, offense, in mice. Behav. Genet. 26: 471-477.Google Scholar
  51. Maxson, S. C., Roubertoux, P. I., Guillot, P.-V., and Goldman, D. (2001). The genetics of aggression: From mice to humans. In M. Martinez (Ed.), Prevention and control of aggression and the impact on the victim (pp. 71-81). New York: Kluwer Academic.Google Scholar
  52. Miczek, K. A., Maxson, S. C., Fish, E. W., and Faccidomo, S. (2001). Aggressive behavioral phenotypes in mice. Behav. Brain Res. 12:167-181.Google Scholar
  53. Moffitt, T. E. (1990). Juvenile delinquency and attention-deficit disorder: Developmental trajectories from age three to fifteen. Child Dev. 61:893-910.Google Scholar
  54. Moffitt, T. E. (1993). “Life-course-persistent” and “adolescencelimited” antisocial behavior: A developmental taxonomy. Psychol. Rev. 100:674-701.Google Scholar
  55. Moffitt, T. E. (2003). Life-course persistent and adolescence-limited antisocial behaviour: A research review and a research agenda. In B. Lahey, T. E. Moffitt, and A. Caspi (Eds.), The causes of conduct disorder and serious juvenile delinquency. New York: Guilford (in press).Google Scholar
  56. Moffitt, T. E., Lynam, D., and Silva, P. A. (1994). Neuropsychological tests predict persistent male delinquency. Criminology 32:101-124.Google Scholar
  57. Moffitt, T. E., Caspi, A., Dickson, N., Silva, P. A., and Stanton, W. (1996). Childhood-onset versus adolescent-onset antisocial conduct in males: Natural history from age 3 to 18. Dev. Psychopathol. 8:399-424.Google Scholar
  58. Moffitt, T. E., Brammer, G., Caspi, A., Fawcett, P., Raleigh, M., Yuwiler, A., and Silva, P. A. (1998). Whole blood serotonin relates to violence in an epidemiological study. Biol. Psych. 43:446-457.Google Scholar
  59. Moffitt, T. E., and Caspi, A. (2001). Childhood predictors differentiate life-course persistent and adolescence-limited pathways, among males and females. Dev. Psychopathol. 13:355-375.Google Scholar
  60. Moffitt, T. E., Caspi, A., Rutter, M., and Silva, P. A. (2001). Sex differences in antisocial behaviour: Conduct disorder, delinquency, and violence in the Dunedin longitudinal study. Cambridge: Cambridge University Press.Google Scholar
  61. Moffitt, T. E., Caspi, A., Harrington, H., and Milne, B. (2002). Males on the life-course persistent and adolescence-limited antisocial pathways: Follow-up at age 26. Dev. Psychopathol. 14:179-206.Google Scholar
  62. Mouse Genome Sequencing Consortium (2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420:520-562.Google Scholar
  63. Nelson, R. J., and Chiavegatto, S. (2001). Molecular basis of aggression. TINS 24:713-719.Google Scholar
  64. Olivier, B., Mos, J., Tulp, M. T. M., Schipper, J., den Daas, S., and van Oortmerssen, G. A. (1990). Serotonergic involvement in aggressive animals. In H. M. van Praag, R. Plutchik, and A. Apter (Eds.), Violence and suicidality (pp. 79-137). New York: Brunner/Mazel.Google Scholar
  65. Plomin, R., Owen, M. J., and McGuffin, P. (1994). The genetic basis of complex human behaviors. Science 264:1733-1739.Google Scholar
  66. Porsolt, R. D., Le Pichon, M., and Jalfre, M. (1977). Depression: A new animal model sensitive to antidepressant treatments. Nature 266:730-732.Google Scholar
  67. Raine, A. (2002). Biosocial studies of antisocial and violent behavior in children and adults: A review. J. Abnorm. Child. Psych. 4:311-326.Google Scholar
  68. Rhee, S., and Waldman, I. D. (2002). Genetic and environmental influences on antisocial behavior: A meta-analysis of twin and adoption studies. Psych. Bull. 128:490-529.Google Scholar
  69. Robins, L. N. (1998). The intimate connection between antisocial personality and substance abuse. Soc. Psychiatry Psychiatr. Epidemiol. 33:393-399.Google Scholar
  70. Rolls, E. T. (2000). Memory systems in the brain. Ann. Rev. Psych. 51:599-630.Google Scholar
  71. Roubertoux, P. L., Carlier, M., Degrelle, H., Haas-Dupertuis, M.-C., Phillips, J., and Moutier, R. (1994). Co-segregation of intermale aggression with the pseudoautosomal region of the Y chromosome in mice. Genet. 136:225-230.Google Scholar
  72. Saudou, F., Amara, D. A., Dierich, A., Lemeur, M., Ramboz, S., Segu, L., Buhot, M.-C., and Hen, R. (1994). Enhanced aggressive behavior in mice lacking 5-HT1B receptor. Science 265:1875-1878.Google Scholar
  73. Seguin, J. R., Arseneault, L., Boulerice, B., Harden, P. W., and Tremblay, R. E. (2002). Response perseveration in adolescent boys with stable and unstable histories of physical aggression: The role of underlying processes. J. Child Psychol. Psychiatry 4:481-494.Google Scholar
  74. Sluyter, F., Jamot, L., van Oortmerssen, G. A., and Crusio, W. E. (1994a). Hippocampal mossy fiber distributions in mice selected for aggression, Brain Res. 646:145-148.Google Scholar
  75. Sluyter, F., van der Vlugt, J. J., van Oortmerssen, G. A., and Wijchman, J. (1994b). Sperm characteristics in two selection lines for attack latency. Behav. Genet. 24:531.Google Scholar
  76. Sluyter, F., Korte, S. M., Bohus, B., and van Oortmerssen, G. A. (1996a). Behavioral stress response of genetically selected aggressive and non-aggressive wild house mice in the shock-probe/defensive burying test. Pharmacol. Biochem. Behav. 54:113-116.Google Scholar
  77. Sluyter, F., van Oortmerssen, G. A., de Ruiter, A. J. H., and Koolhaas, J. M. (1996b). Aggression in wild house house mice: Current state of affairs. Behav. Genet. 26:489-496.Google Scholar
  78. Sluyter, F., van Oortmerssen, G. A., and Koolhaas, J. M. (1996c). Genetic influences on coping behaviour: Effects of the Y chromosome in wild house mouse lines bidirectionally selected for aggression. Behaviour 133:109-119.Google Scholar
  79. Sluyter, F., Marican, C. M. M., Roubertoux, P. L., and Crusio, W. E. (1999). Further phenotypical characterisation of two substrains of C57BL/6J inbred mice differing by a spontaneous single-gene mutation. Behav. Brain Res. 98:39-43.Google Scholar
  80. Sluyter, F., Nyberg, J., te Boekhorst, D., Rijsdijk, F. V., Sandnabba, K., Veenema, A. H., Schalkwyk, L. C., and Koolhaas, J. M. (2002). Aggressive behavior in male mice: Focus on underlying dimensions and Y chromosomal effects. Society for Neuroscience Abstracts.Google Scholar
  81. Taylor, J., Iacono, W. G., and McGue, M. (2000). Evidence for a genetic etiology for early-onset delinquency. J. Abnorm. Psychol. 109:634-643.Google Scholar
  82. van Oortmerssen, G. A., and Bakker, T. C. M. (1981). Artificial selection for short and long attack latencies in wild Mus musculus domesticus. Behav. Genet. 11:115-126.Google Scholar
  83. van Oortmerssen, G. A., and Busser, J. (1989). Studies in wild house mice. III: Disruptive selection on aggression as a possible force in evolution. In P. F. Brain, D. Mainardi, and S. Parmigiani (Eds.), House mouse aggression: A model for understanding the evolution of social behaviour (pp. 87-118). London: Harwood Academic.Google Scholar
  84. van Oortmerssen, G. A., Dijk, D. J., and Schuurman, T. (1987). Studies in wild house mice II: Testosterone and aggression. Horm. Behav. 21:139-152.Google Scholar
  85. van Oortmerssen, G. A., Benus, R. F., and Sluyter, F. (1992). Studies on wild house mice. IV: On the heredity of testosterone and readiness to attack. Aggress. Behav. 18:143-148.Google Scholar
  86. van Riel, E., Meijer, O. C., Veenema, A. H., and Joels, M. (2002). Hippocampal serotonin responses in short and long attack latency mice. J. Neuroendocrinol. 14:234-239.Google Scholar
  87. van Zegeren, K. (1980). Variation in aggressiveness and the regulation of numbers in house mouse populations. Neth. J. Zool. 30:635-770.Google Scholar
  88. Veenema, A. H., Meijer, O. C., de Kloet, R., and Koolhaas, J. M. (2003a). Differences in basal and stress-induced HPA regulation of wild house mice selected for high and low aggression. Horm. Behav. 54:197-204.Google Scholar
  89. Veenema, A. H., Meijer, O. C., de Kloet, R., and Koolhaas, J. M. (2003b). Genetic selection for coping style predicts stressor susceptibility. J. Neuroendocrinol 15:256-267.Google Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • Frans Sluyter
  • Louise Arseneault
  • Terrie E. Moffitt
  • Alexa H. Veenema
  • Sietse de Boer
  • Jaap M. Koolhaas

There are no affiliations available

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