Individual Variation in Aggression of Feral Rodent Strains: A Standard for the Genetics of Aggression and Violence?
Abstract
This article summarizes the broad individual differences in aggressiveness and its relationship with several other behavioral, physiological, and neurobiological characteristics that exist in an outbred laboratory strain of male feral rats. Based on the observations that the individual level of offensive aggressive behavior (i.e., the tendency to defend the home territory) is strongly related to the way they react to various other environmental challenges, it is argued that the individual's level of offensiveness is an important indicator and component of a more traitlike behavioral physiological response pattern (coping strategy) to environmental demands. The coping style of aggressive animals is principally aimed at a (pro)active prevention or manipulation of a stressor, whereas the nonaggressive individuals tend to passively accept or react to it. The (pro)active and reactive/passive behavioral coping styles are clearly associated with distinct patterns of autonomic/endocrine (re)activity and underlying neurobiological correlates and determinants. Consequently, these individual differences in aggression/coping style may not only determine the individual vulnerability to stress-related disease, and hence be an important factor in the population dynamics of the species, but may also determine responsivity to pharmacotherapeutic treatments. From an animal modeling point of view, it is argued that the aggressive extremes of this variation may, under the proper testing conditions, have an enhanced propensity to develop pathological forms of aggression and/or coping, for example, antisocial traits, violence, or impulsivity disorders. Finally, it is proposed that the use of these feral animals as base "material" for genetic association (i.e., QTL search, mRNA differential expression, nucleic acid microarray analysis) and manipulation (i.e., gene silencing or amplification by antisense ODN, siRNA, and/or viral gene-transfer methodologies) studies would most likely be the best option for dissecting successfully the genetic basis of both normal and pathological forms of aggression and/or coping.
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Wild rats from the wild-type Groningen line can be distinguished into three subpopulations characterized by low (<15%), intermediate (15%-55%), and high (>55%) aggression.
“In rats from wild group three subpopulations could be distinguished, which were characterized by low (<15% time spent on aggressive behaviors), intermediate (15%-55%) and high (>55%) aggression.”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [40]
Wistar rats' aggression ranged from 0% to maximally 40% or 50%, with no high-aggression animals observed.
“Distribution of Wistar rats was clearly different, their aggression ranged from 0% to maximally 40% or 50%, with no high-aggression animals observed.”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [40]
Wild rats from the first laboratory-born generation also display play fighting, but less frequently and with slightly different tactics, keeping more distance than laboratory counterparts.
“There is some evidence that wild rats (from the first laboratoryborn generation) also display play fighting, but they do it less frequently and employ slightly different tactics, that is, keeping more distance than their laboratory counterparts.40,41”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [40]
Most research on aggression or domestication was performed in the 1980s.
“Unfortunately, most research on such topics as aggression 188 or domestication 40,41 were performed in the 1980s.”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [40]
Cites
The world report on violence and health
Krug, E. G., Mercy, J. A., Dahlberg, L. L., & Zwi, A. B. (2002) · The Lancet · doi:10.1016/s0140-6736(02)11133-0 · Cited by 9,110 · see citing works
Coping styles in animals: current status in behavior and stress-physiology
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. W., & Blokhuis, H. J. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00026-3 · Cited by 2,875 · cited 3× · see citing works
“The difference in response initiation forms the basis of the terminology we currently use for the different coping strategies in rats and mice, that is, proactive and passive/reactive (see Koolhaas et al., 1999, 2001 for more detailed information).”
BackgroundMethodInfluentialSelf-citationDysfunction in the neural circuitry of emotion regulation–a possible prelude to violence
Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000) · Science · doi:10.1126/science.289.5479.591 · Cited by 1,894 · see citing works
World Report on Violence and Health, World Health Organization
Krug, E. (2002) · Medical Entomology and Zoology · Cited by 1,362 · see citing works
A Comparison of the Social Postures of Some Common Laboratory Rodents
Grant, E. C., & Mackintosh, J. H. (1963) · Behaviour · doi:10.1163/156853963x00185 · Cited by 1,167 · see citing works
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 1× · see citing works
“In another species, the prairie vole, lateral septal vasopressin is strongly related to territorial aggression (Winslow et al., 1993).”
BackgroundConsistent individual differences in early exploratory behaviour of male great tits
Verbeek, M. E. M., Drent, P. J., & Wiepkema, P. R. (1994) · Animal Behaviour · doi:10.1006/anbe.1994.1344 · Cited by 764 · see citing works
Fortschritte der Arzneimittelforschung
Wettstein, A. (1960) · Cellular and Molecular Life Sciences · doi:10.1007/bf02178858 · Cited by 670 · see citing works
Stress, Health, and the Social Environment
Henry, J. P., & STEPHENS, P. M. (1977) · Topics in environmental physiology and medicine · doi:10.1007/978-1-4612-6363-0 · Cited by 608 · see citing works
Aggressive behavior in the rat
Blanchard, R. J., & Blanchard, D. C. (1977) · Behavioral Biology · doi:10.1016/s0091-6773(77)90308-x · Cited by 554 · see citing works
Adaptive individual differences within single populations
Wilson, D. S. (1998) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1998.0202 · Cited by 522 · see citing works
Parallel circuits mediating distinct emotional coping reactions to different types of stress
Keay, K. A., & Bandler, R. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00049-5 · Cited by 512 · see citing works
Young, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R., & Insel, T. R. (1999) · Nature · doi:10.1038/23475 · Cited by 488 · see citing works
Primates--A Natural Heritage of Conflict Resolution
de Waal, F. Β. Μ. (2000) · Science · doi:10.1126/science.289.5479.586 · Cited by 479 · see citing works
Heritable variation for aggression as a reflection of individual coping strategies
Benus, R. F., Bohus, B., Koolhaas, J. M., & van Oortmerssen, G. A. (1991) · Cellular and Molecular Life Sciences · doi:10.1007/bf01923336 · Cited by 478 · see citing works
Self-citationAggressive behavioral phenotypes in mice
Miczek, K. A., Maxson, S. C., Fish, E. W., & Faccidomo, S. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00298-4 · Cited by 448 · see citing works
Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys
Raleigh, M. J., McGuire, M. T., Brammer, G. L., Pollack, D. B., & Yuwiler, A. (1991) · Brain Research · doi:10.1016/0006-8993(91)90001-c · Cited by 447 · see citing works
Nelson, R. J., & Chiavegatto, S. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01996-2 · Cited by 429 · see citing works
Miczek, K. A., Fish, E. W., Bold, J. F. D., & de Almeida, R. M. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1139-6 · Cited by 421 · see citing works
Conditioned defensive burying: A new paradigm for the study of anxiolytic agents
Treit, D., Pinel, J. P. J., & Fibiger, H. C. (1981) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(81)90219-7 · Cited by 420 · see citing works
Stress, Health, and the Social Environment: A Sociobiologic Approach to Medicine
Henry, J. P., & STEPHENS, P. M. (1977) · Medical Entomology and Zoology · Cited by 417 · see citing works
Vasopressin V1b receptor knockout reduces aggressive behavior in male mice
Wersinger, S. R., Ginns, E. I., O'Carroll, A.-M., Lolait, S. J., & Young III, W. S. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001195 · Cited by 397 · see citing works
Brain mechanisms for offense, defense, and submission
Adams, D. B. (1979) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00061926 · Cited by 395 · see citing works
Cerebrospinal Fluid Vasopressin Levels
Coccaro, E. F., Kavoussi, R. J., Hauger, R. L., Cooper, T. B., & Ferris, C. F. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.8.708 · Cited by 392 · see citing works
Defensive burying in rodents: ethology, neurobiology and psychopharmacology
de Boer, S. F., & Koolhaas, J. M. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01278-0 · Cited by 391 · see citing works
Self-citationMehlman, P. T., Higley, J. D., Faucher, I., Lilly, A. A., Taub, D. M., Vickers, J. H., Suomi, S. J., & Linnoila, M. (1994) · American Journal of Psychiatry · doi:10.1176/ajp.151.10.1485 · Cited by 375 · see citing works
(1997) · PubMed · Cited by 350 · see citing works
Self-citationActivity of Serotonergic Neurons in Behaving Animals
Jacobs, B. L. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00012-3 · Cited by 318 · see citing works
Kollack‐Walker, S., & Newman, S. W. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00563-k · Cited by 315 · see citing works
Gregg, T. R., & Siegel, A. (2001) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(00)00150-0 · Cited by 315 · see citing works
Serotonin Receptors and Animal Models of Aggressive Behavior
Olivier, B., Mos, J., van Oorschot, R., & Hen, R. (1995) · Pharmacopsychiatry · doi:10.1055/s-2007-979624 · Cited by 285 · see citing works
Artificial selection for short and long attack latencies in wildMus musculus domesticus
van Oortmerssen, G. A., & Bakker, T. C. M. (1981) · Behavior Genetics · doi:10.1007/bf01065622 · Cited by 263 · see citing works
Veenema, A. H., Meijer, O. C., de Kloet, E. R., Koolhaas, J. M., & Bohus, B. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(02)00013-2 · Cited by 261 · see citing works
Self-citationSocial Stress in Hamsters: Defeat Activates Specific Neurocircuits within the Brain
Kollack‐Walker, S., Watson, S. J., & Akil, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-22-08842.1997 · Cited by 253 · see citing works
Neural Connections of the Anterior Hypothalamus and Agonistic Behavior in Golden Hamsters
Delville, Y., Vries, G. J. D., & Ferris, C. F. (2000) · Brain Behavior and Evolution · doi:10.1159/000006642 · Cited by 251 · see citing works
Cleare, A. J., & Bond, A. J. (1995) · Psychopharmacology · doi:10.1007/bf02245252 · Cited by 241 · see citing works
PSYCHOPHARMACOLOGIC TREATMENT OF PATHOLOGIC AGGRESSION
D, M. F. M. (1997) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(05)70321-x · Cited by 212 · see citing works
Sgoifo, A., de Boer, S. F., Haller, J., & Koolhaas, J. M. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00229-6 · Cited by 206 · see citing works
Self-citationThe organization of intraspecific agonistic behaviour in the rat
KOOLHAAS, J., Schuurman, T., & Wiepkema, P. R. (1980) · Progress in Neurobiology · doi:10.1016/0301-0082(80)90024-6 · Cited by 193 · see citing works
Self-citationDe Vries, G., Wang, Z., Bullock, N., & Numan, S. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01789.1994 · Cited by 193 · see citing works
Genetic Selection For Coping Style Predicts Stressor Susceptibility
Veenema, A. H., Meijer, O. C., de Kloet, E. R., & Koolhaas, J. M. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.00986.x · Cited by 192 · see citing works
Self-citationKorte, S. M. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00149-2 · Cited by 191 · see citing works
Coping with Challenge: Welfare in Animals including Humans
Mendl, M. (2001) · Cited by 188 · see citing works
Vasopressin and serotonin interactions in the control of agonistic behavior
Ferris, C. F., & Delville, Y. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90043-4 · Cited by 172 · see citing works
Lester, H. A. (1977) · Scientific American · doi:10.1038/scientificamerican0277-106 · Cited by 169 · see citing works
Miczek, K. A., Weerts, E. M., Haney, M., & Tidey, J. W. (1994) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)90040-x · Cited by 154 · see citing works
Incidence of arrhythmias and heart rate variability in wild-type rats exposed to social stress
Sgoifo, A., de Boer, S. F., Westenbroek, C., Maes, F. W., Beldhuis, H. J. A., Suzuki, T., & Koolhaas, J. M. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.273.4.h1754 · Cited by 153 · see citing works
Self-citationLore, R., & Flannelly, K. (1977) · Scientific American · doi:10.1038/scientificamerican0577-106 · Cited by 147 · see citing works
Manipulations of dietary tryptophan: Effects on mouse killing and brain serotonin in the rat
Gibbons, J. L., Barr, G. A., Bridger, W. H., & LEIBOWITZ, S. F. (1979) · Brain Research · doi:10.1016/0006-8993(79)90380-9 · Cited by 137 · see citing works
Enhanced 5-HT1A receptor expression in forebrain regions of aggressive house mice
Korte, S. M., Meijer, O. C., de Kloet, E. R., Buwalda, B., Keijser, J. N., Sluyter, F., van Oortmerssen, G. A., & Bohus, B. (1996) · Brain Research · doi:10.1016/0006-8993(96)00723-8 · Cited by 136 · see citing works
Bjork, J. M. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00136-0 · Cited by 135 · see citing works
Differential lateral septal vasopressin innervation in aggressive and nonaggressive male mice
Compaan, J. C., Buijs, R. M., Pool, C. W., De Ruiter, A. J. H., & koolhaas, J. M. (1993) · Brain Research Bulletin · doi:10.1016/0361-9230(93)90032-7 · Cited by 135 · see citing works
Self-citationMedial amygdala and aggressive behavior: Interaction between testosterone and vasopressin
Koolhaas, J. M., Brink, T. H. C. V. D., Roozendaal, B., & Boorsma, F. (1990) · Aggressive Behavior · doi:10.1002/1098-2337(1990)16:3/4 · Cited by 134 · see citing works
Vergnes, M., Depaulis, A., & Boehrer, A. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90349-5 · Cited by 116 · see citing works
Malmberg, T. (1980) · De Gruyter eBooks · doi:10.1515/9783110809442 · Cited by 116 · see citing works
Sluyter, F., Korte, S. M., Bohus, B., & van Oortmerssen, G. A. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02164-7 · Cited by 115 · see citing works
Brain mediation of active and passive emotional coping
Bandler, R. J., Price, J. L., & Keay, K. A. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62149-4 · Cited by 108 · see citing works
Haller, J., van de Schraaf, J., & Kruk, M. R. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00600.x · Cited by 106 · see citing works
The serotonin hypothesis of aggression revisited
Berman, M. E., Tracy, J. I., & Coccaro, E. F. (1997) · Clinical Psychology Review · doi:10.1016/s0272-7358(97)00039-1 · Cited by 105 · see citing works
Cherek, D. R., Lane, S. D., Pietras, C. J., & Steinberg, J. L. (2001) · Psychopharmacology · doi:10.1007/s002130100915 · Cited by 105 · see citing works
Halász, J., Liposits, Z., Kruk, M. R., & Haller, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01883.x · Cited by 105 · see citing works
Selective serotonin reuptake inhibitors and violence: a review of the available evidence
Walsh, M., & Dinan, T. G. (2001) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2001.00357.x · Cited by 104 · see citing works
Differential Lateral Septal Vasopressin in Wild-type Rats: Correlation with Aggression
Everts, H. G. J., de Ruiter, A. J. H., & Koolhaas, J. M. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1375 · Cited by 102 · see citing works
Self-citationTestosterone and its metabolites modulate 5HT1A and 5HT1B agonist effects on intermale aggression
Simon, N. G., Cologer–Clifford, A., Lu, S., McKenna, S., & Hu, S. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00034-7 · Cited by 101 · see citing works
de Boer, S. F., Lesourd, M., Mocaër, E., & Koolhaas, J. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38065-6 · Cited by 100 · see citing works
Self-citationUse of fluoxetine to treat dominance aggression in dogs
Dodman, N. H., Donnelly, R., Shuster, L., Mertens, P. A., Rand, W., & Miczek, K. A. (1996) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1996.209.09.1585 · Cited by 96 · see citing works
Identification of Quantitative Trait Loci That Affect Aggressive Behavior in Mice
Brodkin, E. S., Goforth, S. A., Keene, A. H., Fossella, J., & Silver, L. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-01165.2002 · Cited by 88 · see citing works
de Boer, S. F. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00092-0 · Cited by 88 · see citing works
Ruis, M. A. W., de Groot, J., Brake, J. H. A. T., Ekkel, E. D., van de Burgwal, J. A., Erkens, J. H. F., ENGEL, B., Buist, W. G., Blokhuis, H. J., & Koolhaas, J. M. (2001) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(00)00150-7 · Cited by 88 · see citing works
Self-citationActivation of serotonergic neurotransmission during the performance of aggressive behavior in rats.
van der Vegt, B. J., Lieuwes, N. G., van de Wall, E. H. E. M., Kato, K., Moya‐Albiol, L., Martínez‐Sanchis, S., de Boer, S. F., & Koolhaas, J. M. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.667 · Cited by 84 · see citing works
Self-citationStudies in Wild House Mice: Genotype-Environment Interactions for Attack Latency
Dijk, D., van Oortmerssen, G. A., & Benus, I. (1984) · Netherlands Journal of Zoology · doi:10.1163/002829685x00118 · Cited by 81 · see citing works
Anxiety/aggression - driven depression
van Praag, H. M. (2001) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(01)00151-8 · Cited by 78 · see citing works
Cerebrospinal fluid monoamine and metabolite concentrations and aggression in rats
van der Vegt, B. J., Lieuwes, N. G., Cremers, T. I. F. H., de Boer, S. F., & Koolhaas, J. M. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00132-6 · Cited by 78 · see citing works
Self-citationTuinier, S., Verhoeven, W. M. A., & van Praag, H. M. (1995) · International Clinical Psychopharmacology · doi:10.1097/00004850-199510030-00003 · Cited by 74 · see citing works
Release of vasopressin within the brain contributes to neuroendocrine and behavioral regulation
Landgraf, R., Wotjak, C. T., Neumann, I. D., & Engelmann, M. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61571-x · Cited by 66 · see citing works
Ferris, C. F. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00011.x · Cited by 65 · see citing works
van der Vegt, B. J., de Boer, S. F., Buwalda, B., de Ruiter, A. J. H., de Jong, J. G., & Koolhaas, J. M. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00565-0 · Cited by 65 · see citing works
Self-citationFeldker, D. E. M., Datson, N. A., Veenema, A. H., Meulmeester, E., de Kloet, E. R., & Vreugdenhil, E. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02440.x · Cited by 65 · see citing works
How and why coping systems vary among individuals.
de Boer, S. F., Carere, C., Groothuis, T. G. G., & Broom, D. (2001) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 59 · see citing works
Kavelaars, A., Heijnen, C. J., Tennekes, R., Bruggink, J. E., & Koolhaas, J. M. (1999) · Brain Behavior and Immunity · doi:10.1006/brbi.1998.0534 · Cited by 56 · see citing works
Self-citationMitchell, P. J., & Redfern, P. H. (1997) · Behavioural Pharmacology · doi:10.1097/00008877-199711000-00016 · Cited by 53 · see citing works
Activity of Serotonergic Neurons in Behaving Animals
Jacobs, B. L., & Fornal, C. A. (1999) · Neuropsychopharmacology · doi:10.1038/sj.npp.1395336 · Cited by 42 · see citing works
Mitchell, P. J., & Redfern, P. H. (1992) · Journal of Psychopharmacology · doi:10.1177/026988119200600218 · Cited by 35 · see citing works
Daruna, J. H., & Kent, E. W. (1976) · Brain Research · doi:10.1016/0006-8993(76)90473-x · Cited by 32 · see citing works
Miczek, K. A. (1999) · Psychopharmacology · doi:10.1007/s002130051132 · Cited by 21 · see citing works
Sluyter, F., Korte, S. M., van Baal, G. C. M., de Ruiter, A. J. H., & van Oortmerssen, G. A. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00101-8 · Cited by 21 · see citing works
The effects of age and strain on aggression in male rats
Blanchard, R. J., Flannelly, K. J., Layng, M. P., & Blanchard, D. C. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90219-1 · Cited by 16 · see citing works
Genetic Influences on Aggressive Behavior
Maxson, S. C. (1999) · CRC Press eBooks · doi:10.1201/9781420048223.ch22 · Cited by 15 · see citing works
Human Territoriality: Survey of Behavioural Territories in Man with Preliminary Analysis of Meaning
Peachey, P., & Malmberg, T. (1984) · Anthropological Quarterly · doi:10.2307/3317300 · Cited by 1 · see citing works
Flagged first, then by citations
2 of the 91 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Integrating animal temperament within ecology and evolution
Réale, D. J. F., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2007.00010.x · Cited by 3,587 · see citing works
Korte, S. M., Koolhaas, J. M., Wingfield, J. C., & McEwen, B. S. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.08.009 · Cited by 1,097 · see citing works
“In contrast, aggressive Hawk type individuals appear to be missing from Wistar rat populations, probably because these rats have been genetically selected for easy handling [34].”
BackgroundResultInfluentialSelf-citationNeuroendocrinology of coping styles: Towards understanding the biology of individual variation
Koolhaas, J. M., de Boer, S. F., Coppens, C. M., & Buwalda, B. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.04.001 · Cited by 883 · see citing works
Self-citationCoping styles and behavioural flexibility: towards underlying mechanisms
Coppens, C. M., de Boer, S. F., & Koolhaas, J. M. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2010.0217 · Cited by 610 · see citing works
“…mice differ in the serotonergic input of the PFC. Rats with extensive experience of aggressive behaviour have lower levels of release of serotonin (5-hydroxytryptamine; 5-HT) in the PFC (van Erp & Miczek 2000; De Boer et al. 2003; Ferrari et al. 2003; Caramaschi et al. 2007; Miczek et al. 2007).”
BackgroundSelf-citationEarly life stress and development: potential mechanisms for adverse outcomes
Smith, K. E., & Pollak, S. D. (2020) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-020-09337-y · Cited by 500 · see citing works
Øyvind Øverli, A., Sørensen, C., Pulman, K. G. T., Pottinger, T. G., Korzan, W. J., Summers, C. H., & Nilsson, G. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.10.006 · Cited by 503 · see citing works
“A genetic basis for the expression of behavioral and physiological components of individual coping styles has repeatedly been demonstrated (e.g. Driscoll et al., 1998; Lepage et al., 2000; Ellenbroek and Cools, 2002; de Boer et al, 2003; Veenema et al., 2003).”
BackgroundKoolhaas, J. M., de Boer, S. F., Buwalda, B., & van Reenen, K. (2007) · Brain Behavior and Evolution · doi:10.1159/000105485 · Cited by 440 · see citing works
“…a comparison between the frequency distribution of aggressive behavior in a standard laboratory rat strain with that of laboratory bred wild rats reveals that a considerable number of the more aggressive phenotypes in wild rats are completely absent in the laboratory strain [De Boer et al., 2003].”
BackgroundSelf-citationThe Resident-intruder Paradigm: A Standardized Test for Aggression, Violence and Social Stress
Koolhaas, J. M., Coppens, C. M., de Boer, S. F., Buwalda, B., Meerlo, P., & Timmermans, P. J. A. (2013) · Journal of Visualized Experiments · doi:10.3791/4367 · Cited by 391 · see citing works
Self-citationSmith, K. E., & Pollak, S. D. (2020) · Perspectives on Psychological Science · doi:10.1177/1745691620920725 · Cited by 351 · see citing works
Øverli, Ø. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.3.463 · Cited by 348 · see citing works
“A genetic basis for the expression of behavioral and physiological components of individual coping styles has repeatedly been demonstrated (e.g., Driscoll et al., 1998; Ellenbroek and Cools, 2002; de Boer et al., 2003; Veenema et al., 2003).”
Backgroundde Boer, S. F., & Koolhaas, J. M. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.065 · Cited by 320 · see citing works
Self-citationCoping style and immunity in animals: Making sense of individual variation
Koolhaas, J. M. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.11.006 · Cited by 300 · see citing works
“The results of a series of experiments not only in mice but also in feral rats, demonstrate that the individual tendency to initiate aggressive behavior is indeed predictive for the individual reaction to other, non-social environmental challenges (De Boer and Koolhaas, 2003; De Boer et al., 2003).”
BackgroundSelf-citationVeenema, A. H. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.003 · Cited by 268 · see citing works
McDougall, P. T., Réale, D., Sol, D., & Reader, S. M. (2006) · Animal Conservation · doi:10.1111/j.1469-1795.2005.00004.x · Cited by 341 · see citing works
Carere, C., Caramaschi, D., & Fawcett, T. W. (2010) · Current Zoology · doi:10.1093/czoolo/56.6.728 · Cited by 259 · see citing works
“In laboratory Wistar rats, measurable aggression may be very low, rendering these types of studies difficult because of a lack of such behaviour in their agonistic repertoire (de Boer et al., 2003).”
BackgroundSerotonin: A never-ending story
Olivier, B. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.10.031 · Cited by 253 · see citing works
“A recent approach to unraveling the role of the 5-HT system in aggression is studying the differences between highly aggressive and low-aggressive individuals as has been pursued by the group of Koolhaas (de Boer et al., 2003).”
BackgroundNrf2-dependent persistent oxidative stress results in stress-induced vulnerability to depression
Bouvier, E., Brouillard, F., Molet, J., Claverie, D., Cabungcal, J.-H., Cresto, N., Doligez, N., Rivat, C., Do, K. Q., Bernard, C., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.144 · Cited by 248 · see citing works
Neurobiology of Escalated Aggression and Violence
Miczek, K. A., de Almeida, R. M. M., Kravitz, E. A., Rissman, E. F., de Boer, S. F., & Raine, A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3500-07.2007 · Cited by 242 · see citing works
Aggression and anxiety: social context and neurobiological links
Neumann, I. D. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00012 · Cited by 238 · see citing works
“In an out-bred laboratory strain of wild-type rats, a wide range of aggressive behaviours was observed, although individuals with extremes in aggressive behaviour did not differ in anxiety-related behaviours (de Boer et al., 2003).”
BackgroundNormal and abnormal aggression: human disorders and novel laboratory models
Haller, J., & Kruk, M. R. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.01.005 · Cited by 235 · see citing works
Veenema, A. H., Beiderbeck, D. I., Lukas, M., & Neumann, I. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.006 · Cited by 180 · see citing works
“…system in a single brain region might be insufficient to induce or enhance a highly complex behavior like aggression, especially in a rat strain that generally demonstrate low to moderate levels of intermale aggression as compared to other rat strains (De Boer et al., 2003; Veenema et al., 2007b).”
BackgroundThe social life of Norway rats (Rattus norvegicus)
Schweinfurth, M. K. (2020) · eLife · doi:10.7554/elife.54020 · Cited by 176 · see citing works
de Boer, S. F., Buwalda, B., & Koolhaas, J. M. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.008 · Cited by 163 · see citing works
“Rats with extensive experience of aggressive behavior have profoundly lower levels and/or release of 5-HT in the PFC (Van Erp and Miczek, 2000; De Boer et al., 2003; Ferrari et al., 2003; Caramaschi et al., 2007; Miczek et al., 2007).”
BackgroundResultInfluentialSelf-citationEffects of Adverse Early‐Life Events on Aggression and Anti‐Social Behaviours in Animals and Humans
Haller, J., Harold, G. T., Sandi, C., & Neumann, I. D. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12182 · Cited by 168 · see citing works
Indirect genetic effects and the evolution of aggression in a vertebrate system
Wilson, A. J., Gélin, U., Perron, M.-C., & Réale, D. J. F. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.1193 · Cited by 162 · see citing works
Unfolding personalities: The importance of studying ontogeny
Groothuis, T. G. G., & Trillmich, F. (2011) · Developmental Psychobiology · doi:10.1002/dev.20574 · Cited by 161 · see citing works
Olivier, B. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.022 · Cited by 157 · see citing works
Haller, J., Tóth, M., Halász, J., & de Boer, S. F. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.030 · Cited by 148 · see citing works
“Highly aggressive wild type rats also showed abnormal forms of aggressiveness (they disregarded social signals by opponents) when repeatedly exposed to aggressive encounters [24,25].”
BackgroundSocial behavior and social stress in adolescence: A focus on animal models
Buwalda, B., Geerdink, M., Vidal, J., & Koolhaas, J. M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.004 · Cited by 149 · see citing works
Self-citationToth, M., Mikics, E., Tulogdi, A., Aliczki, M., & Haller, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.003 · Cited by 152 · see citing works
“…manipulations, frustration or instigation, genetic selection or the repeated exposure of feral rodents to aggressive encounters (de Almeida and Miczek, 2002; de Boer et al., 2003; Haller and Kruk, 2006; Haller et al., 2001; Miczek et al., 2002; Natarajan et al., 2009; Neumann et al., 2010).”
BackgroundInfluential5-HT1B receptors and aggression: A review
Olivier, B., & van Oorschot, R. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.066 · Cited by 146 · see citing works
“A recent approach to unraveling the role of the 5-HT system in aggression is studying the differences between highly aggressive and low-aggressive individuals as has recently been pursued by the group of Koolhaas (de Boer et al., 2003).”
Ecological validity of social interaction tests in rats and mice
Kondrakiewicz, K., Kostecki, M., Szadzińska, W., & Knapska, E. (2019) · Genes, Brain and Behavior · doi:10.1111/gbb.12525 · Cited by 136 · see citing works
“For example, wild-type Groningen (WTG) line of rats was compared with Wistar rats in terms of aggressive behaviors.(40) Percent of time spent on aggressive behaviors was measured during the Resident-Intruder test.”
BackgroundMethodIndividual coping characteristics, aggressiveness and fighting strategies in pigs
Bolhuis, J. E., Schouten, W. G. P., Schrama, J. W., & Wiegant, V. M. (2005) · Animal Behaviour · doi:10.1016/j.anbehav.2004.09.013 · Cited by 136 · see citing works
Mikics, É., Barsy, B., Barsvári, B., & Haller, J. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.02.002 · Cited by 131 · see citing works
“Two main coping styles have been observed in various species: active (or proactive) coping that correlates with enhanced noradrenaline stress responses, and passive (or reactive) coping that correlates with enhanced corticosterone responses (Carere et al., 2003; De Boer et al., 2003; Koolhaas et al., 1999; Schouten an…”
BackgroundSerotonin and aggressive behavior in rodents and nonhuman primates: Predispositions and plasticity
Ferrari, P. F., Palanza, P., Parmigiani, S., de Almeida, R. M. M., & Miczek, K. A. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.10.002 · Cited by 116 · see citing works
“…strains of mice, recombinant lines or selected lines in order to map or identify genes for aggressive behavior, and to determine the mechanisms through which genes influence aggression (see Brain et al., 1989; Maxson, 1981; Parmigiani et al., 1999; de Boer et al., 2003; Miczek et al., 2001).”
BackgroundKeifer, J., & Summers, C. H. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2016.00069 · Cited by 112 · see citing works
“…deprived with respect to sensory input and behavioral opportunities (Van de Weerd et al., 1997; Kavelaars et al., 1999; van den Berg et al., 1999; de Boer et al., 2003; Meeusen, 2005; Korte et al., 2007; Balcombe, 2010; Blanchard, 2010; MacGillivray et al., 2012; König et al., 2015; Smith et…”
BackgroundIndividual differences in cognition among teleost fishes
Lucon‐Xiccato, T., & Bisazza, A. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2017.01.015 · Cited by 113 · see citing works
Beiderbeck, D. I., Reber, S. O., Havasi, A., Bredewold, R., Veenema, A. H., & Neumann, I. D. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.04.011 · Cited by 109 · see citing works
Minimizing fear and anxiety in working dogs: A review
Rooney, N. J., Clark, C. C. A., & Casey, R. A. (2016) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2016.11.001 · Cited by 111 · see citing works
“Proactive and reactive types of responding have been well documented in laboratory rodents (de Boer et al., 2003) and in other species (see review, Koolhaas et al., 1999; but see also Forkman et al., 1995, and Jensen et al., 1995).”
BackgroundCaramaschi, D., de Boer, S. F., VRIES, H. D., & Koolhaas, J. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.01.003 · Cited by 107 · see citing works
“In such experiments, aggression increases in terms of duration and frequency, while attack latency decreases [31].”
Self-citationTesting for the presence of coping styles in a wild mammal
Ferrari, C., Pasquaretta, C., Carere, C., Cavallone, E., von Hardenberg, A., & Réale, D. J. F. (2013) · Animal Behaviour · doi:10.1016/j.anbehav.2013.03.030 · Cited by 105 · see citing works
Rodent models of social stress and neuronal plasticity: Relevance to depressive-like disorders
Patel, D., Kas, M. J., Chattarji, S., & Buwalda, B. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111900 · Cited by 105 · see citing works
Buwalda, B., Scholte, J. C. M., de Boer, S. F., Coppens, C. M., & Koolhaas, J. M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.012 · Cited by 105 · see citing works
“Male WTG rats differ widely in their offensive aggression (see for a full description of the aggressive behavior of WTG rats de Boer et al., 2003).”
BackgroundSelf-citationde Boer, S. F. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.052.2009 · Cited by 104 · see citing works
“Moreover, local tissue as well as microdialysate levels of 5-HT and 5-HIAA in the frontal cortex did not differ signifi cantly between high- and low-aggressive animals, although there was a slight tendency for lower levels in high-aggressive animals (de Boer et al., 2003; Figure 3).”
Veenema, A. H., Torner, L., Blume, A., Beiderbeck, D. I., & Neumann, I. D. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.07.004 · Cited by 102 · see citing works
Escalated Aggressive Behavior: New Pharmacotherapeutic Approaches and Opportunities
Miczek, K. A., Faccidomo, S., de Almeida, R. M. M., Bannai, M., Fish, E. W., & DeBold, J. F. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.021 · Cited by 95 · see citing works
Excessive aggression as model of violence: a critical evaluation of current preclinical methods
Miczek, K. A., de Boer, S. F., & Haller, J. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3008-x · Cited by 109 · see citing works
“Most likely, this is the result of artificial selection for tame and tractable behavior during the century-long domestication process of these wild-caught animals, being kept, reared, and bred in captivity (Barnett 1963; Boice 1973; de Boer et al. 2003; King 1939; Plyusnina et al. 2011 ).”
BackgroundMechanisms differentiating normal from abnormal aggression: Glucocorticoids and serotonin
Haller, J., Mikics, É., Halász, J., & Tóth, M. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.064 · Cited by 93 · see citing works
Calcagnoli, F., Kreutzmann, J. C., de Boer, S. F., Althaus, M., & Koolhaas, J. M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.09.019 · Cited by 92 · see citing works
Self-citationAntiaggressive activity of central oxytocin in male rats
Calcagnoli, F., de Boer, S. F., Althaus, M., den Boer, J. A., & Koolhaas, J. M. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3124-7 · Cited by 90 · see citing works
Self-citationPotentiation of Divergent Medial Amygdala Pathways Drives Experience-Dependent Aggression Escalation
Nordman, J. C., Ma, X., Gu, Q., Potegal, M., Li, H., Kravitz, A. V., & Li, Z. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0370-20.2020 · Cited by 87 · see citing works
“…offensive aggressive behaviors as reported in previous studies, such as rear and lateral attacks, boxing, chasing, and wrestling (which includes pin downs and clinch attacks) (Blanchard and Blanchard, 1977, 2003a,b; Miczek and O’Donnell, 1978; Potegal et al., 1996b; de Boer et al., 2003) (Fig.”
BackgroundCalcagnoli, F., de Boer, S. F., Beiderbeck, D. I., Althaus, M., Koolhaas, J. M., & Neumann, I. D. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.12.050 · Cited by 84 · see citing works
Self-citationThe socially stressed heart. Insights from studies in rodents
Sgoifo, A., Carnevali, L., & Grippo, A. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.12.005 · Cited by 83 · see citing works
Brunelli, S. A., & Hofer, M. A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.014 · Cited by 80 · see citing works
The neural background of hyper-emotional aggression induced by post-weaning social isolation
Tóth, M., Tulogdi, Á., Bíró, L., Sörös, P., Mikics, É., & Haller, J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.025 · Cited by 79 · see citing works
Selective Breeding for an Infant Phenotype: Rat Pup Ultrasonic Vocalization (USV)
Brunelli, S. A. (2005) · Behavior Genetics · doi:10.1007/s10519-004-0855-6 · Cited by 80 · see citing works
Delineation of Violence from Functional Aggression in Mice: An Ethological Approach
Natarajan, D., VRIES, H. D., Saaltink, D., de Boer, S. F., & Koolhaas, J. M. (2008) · Behavior Genetics · doi:10.1007/s10519-008-9230-3 · Cited by 77 · see citing works
“De Boer et al. (2003) demonstrated the existence of similar phenotypes however, in unselected feral rats.”
ResultSelf-citationSocial environment determines the long-term effects of social defeat
de Jong, J. G., van der Vegt, B. J., Buwalda, B., & Koolhaas, J. M. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.10.013 · Cited by 79 · see citing works
“We used males of an unselected strain of wild type rats (Wildtype Groningen, WTG) because of their high levels of social activity [31].”
BackgroundMethodSelf-citationAttentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task
Patel, S., Stolerman, I. P., Asherson, P. J., & Sluyter, F. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.02.019 · Cited by 78 · see citing works
Calcagnoli, F., Stubbendorff, C., Meyer, N., de Boer, S. F., Althaus, M., & Koolhaas, J. M. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.012 · Cited by 77 · see citing works
Self-citationHeritability of dominant–aggressive behaviour in English Cocker Spaniels
Pérez-Guisado, J., Lopez-Rodríguez, R., & Muñoz-Serrano, A. (2005) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2005.11.005 · Cited by 74 · see citing works
A, T. R. D. J., & Neumann, I. D. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_13 · Cited by 74 · see citing works
Deep evolutionary conservation of autism-related genes
Shpigler, H. Y., Saul, M. C., Corona, F., Block, L. N., Cash-Ahmed, A. C., Zhao, S. D., & Robinson, G. E. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708127114 · Cited by 70 · see citing works
“In addition, individuals within the same species differ in social responsiveness, with well-documented variation among humans (1), primates (2), and other mammals (3).”
BackgroundAnti-aggressive effects of agonists at 5-HT1B receptors in the dorsal raphe nucleus of mice
Bannai, M., Fish, E. W., Faccidomo, S., & Miczek, K. A. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0780-5 · Cited by 71 · see citing works
“As preclinical procedures are advanced to uncover aberrant patterns of aggression (Haller and Kruk 2006; de Boer et al. 2003; Miczek et al. 2002), several methods now exist for studying detailed drug effects on aggression.”
The neurobiology of offensive aggression: Revealing a modular view
de Boer, S. F., Olivier, B., Veening, J., & Koolhaas, J. M. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.040 · Cited by 70 · see citing works
Self-citationNatarajan, D. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00009 · Cited by 66 · see citing works
“Van der Vegt et al. (2003) and de Boer et al. (2003) showed a positive correlation between 5-hydroxyindoleacetic acid (5-HIAA) levels and aggression in wild-type Groningen (WTG) rats, in contrast to human data where low 5-HIAA levels are associated with impulsivity and suicidal behaviors (Asberg et…”
BackgroundResultAnimal models of excessive aggression: implications for human aggression and violence
de Boer, S. F. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.04.006 · Cited by 63 · see citing works
Buwalda, B., Stubbendorff, C., Zickert, N., & Koolhaas, J. M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.050 · Cited by 62 · see citing works
“The male aggressive WTG’s were selected on their high offensive aggression toward an intruder in the resident–intruder paradigm (de Boer et al., 2003).”
Self-citationCoppens, C. M., Siripornmongcolchai, T., Wibrand, K., Alme, M. N., Buwalda, B., de Boer, S. F., Koolhaas, J. M., & Bramham, C. R. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00072 · Cited by 61 · see citing works
“It has been shown that this broad individual variation in aggressiveness can be considered more generally as a variation in actively coping with environmental challenges (De Boer et al., 2003).”
Self-citationA, T. R. D. J., Beiderbeck, D. I., & Neumann, I. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091701 · Cited by 61 · see citing works
Volgin, A. D., Yakovlev, O. A., Demin, K. A., de Abreu, M. S., Alekseeva, P. A., Friend, A. J., Lakstygal, A. M., Amstislavskaya, T. G., Bao, W., Song, C., et al. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24337 · Cited by 59 · see citing works
Territory owners discriminate between aggressive and nonaggressive neighbours
Hyman, J., & Hughes, M. (2006) · Animal Behaviour · doi:10.1016/j.anbehav.2006.01.007 · Cited by 53 · see citing works
Toward an Animal Model for Antisocial Behavior: Parallels Between Mice and Humans
Sluyter, F., Arseneault, L., Moffitt, T. E., Veenema, A. H., de Boer, S. F., & Koolhaas, J. M. (2003) · Behavior Genetics · doi:10.1023/a:1025730901955 · Cited by 55 · see citing works
Self-citationLearning strategies during fear conditioning
Carpenter, R. E., & Summers, C. H. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.01.009 · Cited by 53 · see citing works
Rats Benefit from Winner and Loser Effects
Lehner, S. R., Rutte, C., & Michael Taborsky, A. (2011) · Ethology · doi:10.1111/j.1439-0310.2011.01962.x · Cited by 53 · see citing works
“These rats descended from four pairs of wild-trapped animals that have been outbred in the Groningen laboratory for 25 generations (de Boer et al. 2003).”
BackgroundRapid loss of antipredatory behaviour in captive-bred birds is linked to current avian invasions
Carrete, M., & Tella, J. L. (2015) · Scientific Reports · doi:10.1038/srep18274 · Cited by 53 · see citing works
Repeatability and Heritability of Behavioural Types in a Social Cichlid
Chervet, N., Zöttl, M., Schürch, R., Michael Taborsky, A., & Heg, D. (2011) · International Journal of Evolutionary Biology · doi:10.4061/2011/321729 · Cited by 51 · see citing works
Vidal, J., Buwalda, B., & Koolhaas, J. M. (2011) · Behavioural Processes · doi:10.1016/j.beproc.2011.08.005 · Cited by 50 · see citing works
Self-citationKoolhaas, J. M. (2010) · Wiley eBooks · doi:10.1002/9781444318777.ch22 · Cited by 49 · see citing works
Self-citationEffect of Domestication on Aggression in Gray Norway Rats
Plyusnina, I. Z., Solov’eva, M. Y., & Oskina, I. N. (2011) · Behavior Genetics · doi:10.1007/s10519-010-9429-y · Cited by 49 · see citing works
“Artificial selection, the absence of natural selection pressure, domestication, and inbreeding were all implicated as causes of elimination of high aggression in laboratory rats (De Boer et al. 2003; Koolhaas et al. 2010).”
BackgroundResultInfluentialCalcagnoli, F., Meyer, N., de Boer, S. F., Althaus, M., & Koolhaas, J. M. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.03.008 · Cited by 49 · see citing works
“As compared to commonly used laboratory strains of rats, WTG rats display a much larger variation in the level of intermale offensive aggression (de Boer et al., 2003) and they are therefore a suitable model for clinical aggression research.”
MethodSelf-citationIndividual variation by self-organisation
Hemelrijk, C. K., & Wantia, J. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.07.003 · Cited by 47 · see citing works
“Whereas, some individuals attack only if an opponent is clearly seen to be inferior [48], others attack always (compare the short latency of attack in mice and birds, [49, 50 ].”
BackgroundNeurobehavioral Tests in Rat Models of Degenerative Brain Diseases
Urbach, Y. K., Bode, F. J., Nguyen, H. P., Rieß, O., & von Hörsten, S. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-389-3_24 · Cited by 46 · see citing works
Play, variation in play and the development of socially competent rats
Himmler, S. M., Himmler, B. T., Pellis, V. C., & Pellis, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003307 · Cited by 57 · see citing works
Vagal Withdrawal and Susceptibility to Cardiac Arrhythmias in Rats with High Trait Aggressiveness
Carnevali, L., Trombini, M., Porta, A., Montano, N., de Boer, S. F., & Sgoifo, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068316 · Cited by 48 · see citing works
Zebrafish models: do we have valid paradigms for depression?
de Abreu, M. S., Friend, A. J., Demin, K. A., Amstislavskaya, T. G., Bao, W., & Kalueff, A. V. (2018) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2018.07.002 · Cited by 45 · see citing works
Social Regulation of Neurogenesis in Teleosts
Sørensen, C., Øverli, Ø., Summers, C. H., & Nilsson, G. (2007) · Brain Behavior and Evolution · doi:10.1159/000105487 · Cited by 44 · see citing works
“It has, however, also been firmly established that coping style has a genetic component [Driscoll et al., 1998; Koolhaas et al., 1999; Lepage et al., 2000; Ellenbroek and Cools, 2002; de Boer et al., 2003; Veenema et al., 2003].”
BackgroundAnxiety Profiles of Mice Selectively Bred for Intermale Aggression
Nyberg, J. M., Vekovischeva, O. Y., & Sandnabba, N. K. (2003) · Behavior Genetics · doi:10.1023/a:1025718531997 · Cited by 43 · see citing works
Fargallo, J. A., Velando, A., López‐Rull, I., Ganan, N., Lifshitz, N., Wakamatsu, K., & Torres, R. (2013) · Behavioral Ecology · doi:10.1093/beheco/art088 · Cited by 41 · see citing works
The Nrf2 Pathway in Depressive Disorders: A Systematic Review of Animal and Human Studies
Sani, G., Margoni, S., Brugnami, A., Ferrara, O. M., Bernardi, E., Simonetti, A., Monti, L., Mazza, M., Janiri, D., Moccia, L., et al. (2023) · Antioxidants · doi:10.3390/antiox12040817 · Cited by 41 · see citing works
Kruk, M. R. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_313 · Cited by 38 · see citing works
Calfa, G. D., Volosin, M., & Molina, V. A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.022 · Cited by 36 · see citing works
Liu, Q., Qin, J., Qin, C. H. E. N., Wang, D., & Shi, D. (2012) · Integrative Zoology · doi:10.1111/j.1749-4877.2012.00296.x · Cited by 34 · see citing works
“…and aggression is important in determining the reproductive success and regulation of the density of animals depending on ecological conditions, such as quality, quantity, and distribution of food in habitat (e.g. Barnett 1975; Brown 1975; Wittenberger 1981; Benus et al. 1991; de Boer et al. 2003).”
BackgroundMale Norway rats cooperate according to direct but not generalized reciprocity rules
Schweinfurth, M. K., Aeschbacher, J., Santi, M., & Michael Taborsky, A. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.03.015 · Cited by 32 · see citing works
Fish, E. W., McKenzie-Quirk, S. D., Bannai, M., & Miczek, K. A. (2007) · Psychopharmacology · doi:10.1007/s00213-007-1017-3 · Cited by 32 · see citing works
Nyberg, J., Sandnabba, K. N., Schalkwyk, L. C., & Sluyter, F. (2003) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2003.0056.x · Cited by 31 · see citing works
“These data add weight to the concept of two fundamentally different, heritable behavioral strategies in rodents (Benus et al. 1991; De Boer & Koolhaas 2003; De Boer et al. 2003; Koolhaas et al. 1999).”
BackgroundHigher BDNF concentrations in the hippocampus and cortex of an aggressive mouse strain
Lang, U. E., Günther, L., SCHEUCH, K., KLEIN, J., Eckhart, S. G., Hellweg, R., Danker‐Hopfe, H., & Oehler, J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.08.025 · Cited by 31 · see citing works
Correlated Behavioral Traits in Rats of the Roman Selection Lines
Coppens, C. M., de Boer, S. F., Steimer, T. J., & Koolhaas, J. M. (2013) · Behavior Genetics · doi:10.1007/s10519-013-9588-8 · Cited by 30 · see citing works
Self-citationde Boer, S. F., & Newman‐Tancredi, A. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4173-x · Cited by 30 · see citing works
“An extensive description of the different behavioural elements displayed during agonistic interactions has been reported previously (Koolhaas et al. 2013; de Boer et al. 2003).”
BackgroundAggressive behavior: Implications of dominance and subordination for the study of mental disorders
Arregi, A., Azpiroz, A., Fano, E., & Garmendia, L. (2006) · Aggression and Violent Behavior · doi:10.1016/j.avb.2006.01.005 · Cited by 30 · see citing works
- Authors
- de Boer, S. F., van der Vegt, B. J., & Koolhaas, J. M.
- Venue
- Behavior Genetics
- Published
- 2003-09
- Volume
- 33
- Issue
- 5
- Pages
- 485-501
- ISSN
- 0001-8244 (ISSN-L)
- 1573-3297
- OpenAlex
- W2151519006
- Cited by
- 219
- References
- 91
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 9 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 11 · 2019: 8 · 2018: 7 · 2017: 15 · 2016: 16 · 2015: 6 · 2014: 19 · 2013: 12 · 2012: 7
- FWCI
- 3.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Behavior Genetics (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- aggression, individual differences, coping styles, proactive coping, reactive coping, stress response, neurobiology of aggression, antisocial behavior, impulse control disorders, genetic association, quantitative trait loci, gene silencing, antisense oligonucleotides, viral gene delivery
- MeSH terms
- Aggression, Animals, Animals, Wild, Catecholamines, Corticosterone, Female, Housing, Animal, Male, Reaction Time, Genetic Variation, Rats
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