The DOI matches its Crossref record; 89 of the 91 references it cites were found in a registry or an index.
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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“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
Citations
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
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×
“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
World Report on Violence and Health, World Health Organization
Eg, K. (2002) · Medical Entomology and Zoology · Cited by 1,356
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
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×
“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
Fortschritte der Arzneimittelforschung
Wettstein, A. (1960) · Cellular and Molecular Life Sciences · doi:10.1007/bf02178858 · Cited by 670
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
Aggressive behavior in the rat
Blanchard, R. J., & Blanchard, D. C. (1977) · Behavioral Biology · doi:10.1016/s0091-6773(77)90308-x · Cited by 560
Flagged first, then by citations
2 of the 91 references couldn’t be matched to a known paper.
Research works printed but not linked: 12
- Barnett, S. A. (1975). The rat: A study of behavior. Chicago: The University of Chicago Press.
- Coccaro, E. F., and Kavoussi, R. J. (1996). Neurotransmitter correlates of aggression. In D. M. Stoff and R. B. Cairns (Eds.). The neurobiology of clinical aggression (pp. 67-85). Mahwah, NJ: Lawrence J. Erlbaum Associates Inc.
- de Boer, S. F., van der Vegt, B. J., and Koolhaas, J. M. (2001). Hypersensitivity of 5-HT1A and 5-HT1B autoreceptors as a causal neuromechanism underlying high trait aggressiveness. Soc. Neurosci. Abstr. 89:7.
- Koolhaas, J. M., Moor, E., Hiemstra, Y., and Bohus, B. (1991). The testosterone dependent vasopressinergic neurons in the medial amygdala and lateral septum: Involvement in social behavior of male rats. In S. Jard and R. Jamison (Ed.), Vasopressin (pp. 213-219). Paris-London: Inserm/John Libbey Eurotexty Ltd.
- Menard, J. L., and Meaney, M. J. (2001). Maternal care in early life influences patterns of defensive responding and associated fos expression in adulthood. Soc. Neurosci. Abstr. 541:4.
- Olivier, B., Mos, J., Raghoebar, M., de Koning, P., and Mak, M. (1994). Serenics. In E. Jucker (Eds.), Progress in drug research (Vol. 42, pp. 167-308). Basel: Birkhauser Verlag.
- Scott, J. P. (1958). Aggression. Chicago: The University of Chicago Press.
- Smit, J., van Oosten, R. V., Palm, I. F., Doze, P., Koolhaas, J. M., and Zaagsma, J. (1998). Prejunctional modulation of noradrenergic neurotransmission in wild type rats: A possible relationship with coping styles. Am. J. Physiol. 7:111-122.
- Timmermans, P. J. A. (1978). Social behavior in the rat. PhD thesis. University of Nijmegen.
- van Hooff, J. A. R. A. M. (1977). The adaptive meaning of aggressive behavior. In P. R. Wiepkema and J. A. R. A. M. van Hooff (Eds.), Aggressive behavior: Causes and functions. Utrecht: Bohn, Scheltema and Holkema.
- van Oortmerssen, G. A., and Busser, J. (1989). 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 behavior (pp. 87-116). Chur: Harwood Academic.
- Wilson, E. A. (1975). Sociobiology. Cambridge: Belknap Press, Harvard University Press.
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Items 101–200 of 219
Studies into abnormal aggression in humans and rodents: Methodological and translational aspects
Haller, J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.022 · Cited by 32
Hormonal and neurochemical mechanisms of aggression and a new classification of aggressive behavior
Chichinadze, K., Chichinadze, N., & Lazarashvili, A. (2011) · Aggression and Violent Behavior · doi:10.1016/j.avb.2011.03.002 · Cited by 29
Conspecific Interactions in Adult Laboratory Rodents: Friends or Foes?
Lukas, M., & A, T. R. D. J. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_428 · Cited by 29
Evolution of stress responses refine mechanisms of social rank
Korzan, W. J., & Summers, C. H. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100328 · Cited by 30
“There have also been studies on aggression in captured feral rodents (Benus et al., 1991; de Boer et al., 2003; Everts et al., 1997; Sgoifo et al., 1996).”
BackgroundKorte, S. M., Prins, J., Vinkers, C. H., & Olivier, B. (2009) · The Veterinary Journal · doi:10.1016/j.tvjl.2009.08.023 · Cited by 30
“Hawks with their relatively low corticosteroid levels and high testosterone concentrations have a higher predisposition to express aggressive behaviour, but the trade-off is an increased incidence of antisocial behaviour and reduced cooperation, violent behaviour and injury (De Boer et al., 2003).”
BackgroundDopamine, Glutamate, and Aggression
Miczek, K. A., & Fish, E. W. (2005) · Humana Press eBooks · doi:10.1007/978-1-59259-852-6_11 · Cited by 27
Peeters, D., de Boer, S., Terneusen, A., Newman-Tancredi, A., Varney, M., Verkes, R., & Homberg, J. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.05.004 · Cited by 24
“An extensive description of the different behavioral elements displayed during agonistic interactions has been reported previously (De Boer et al., 2003; Koolhaas et al., 2013) Briefly, the following behavioral elements are distinguished: 1) lateral threat; 2) keep down; 3) clinch attack; 4) chase;…”
BackgroundVidal, J., Buwalda, B., & Koolhaas, J. M. (2011) · Behavioural Processes · doi:10.1016/j.beproc.2011.03.004 · Cited by 28
Self-citationTakahashi, A., Shiroishi, T., & Koide, T. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00156 · Cited by 26
“The aggressive behavior of wild rodents is also more intense and more diversified than that of laboratory rodents (de Boer et al., 2003).”
BackgroundHe, L., Li, L.-H., Wang, W., Liu, G., Liu, S., Liu, W., & Hu, D. (2014) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2014.03.011 · Cited by 25
Stryjek, R., Parsons, M. H., Fendt, M., Święcicki, J., & Bębas, P. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109303 · Cited by 24
Transcriptomic underpinnings of high and low mirror aggression zebrafish behaviours
Reichmann, F., Pilic, J., Trajanoski, S., & Norton, W. (2022) · BMC Biology · doi:10.1186/s12915-022-01298-z · Cited by 23
“varying levels of aggression depending upon their dominance status, and intrinsic factors such as size, fitness, or metabolic status [2, 3].”
BackgroundCarnevali, L., Nalivaiko, E., & Sgoifo, A. (2014) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2014.07.003 · Cited by 24
Trait aggressiveness does not predict social dominance of rats in the Visible Burrow System
Buwalda, B., Koolhaas, J. M., & de Boer, S. F. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.01.008 · Cited by 24
Self-citationNeuroendocrine and Autonomic Correlates of Animal Personalities
Caramaschi, D., Carere, C., Sgoifo, A., & Koolhaas, J. M. (2013) · University of Chicago Press eBooks · doi:10.7208/chicago/9780226922065.003.0013 · Cited by 23
Self-citationSocial housing influences the composition of volatile compounds in the preputial glands of male rats
Pohorecky, L. A., Blakley, G. G., Ma, E. W., Soini, H. A., Wiesler, D. P., Bruce, K. E., & Novotný, M. V. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.12.006 · Cited by 24
“It is generally accepted that rats differ in innate aggression (de Boer et al., 2003).”
BackgroundStress Coping Styles and Singing Behavior in the Short-Tailed Singing Mouse (Scotinomys Teguina)
Crino, O. L., Larkin, I., & Phelps, S. M. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.02.011 · Cited by 23
“The magnitude of the stress response varies greatly between individuals in many taxa, including rodents (De Boer et al., 2003), pigs (Ruis et al., 2001), birds (Marchetti and Drent, 2000), fish (Dingemanse et al., 2007; Schojolden et al., 2005; Ward et al., 2004), and humans (Tyrka et al., 2006).”
Gene expression profiles underlying aggressive behavior in the prefrontal cortex of cattle
Eusebi, P. G., Sevane, N., O’Rourke, T., Pizarro, M., Boeckx, C., & Dunner, S. (2021) · BMC Genomics · doi:10.1186/s12864-021-07505-5 · Cited by 24
Quantitative standardization of resident mouse behavior for studies of aggression and social defeat
Kwiatkowski, C. C., Akaeze, H., Ndlebe, I., Goodwin, N. L., Eagle, A. L., Moon, K., Bender, A. R., Golden, S. A., & Robison, A. J. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01018-1 · Cited by 21
Denial of Reward in the Neonate Shapes Sociability and Serotonergic Activity in the Adult Rat
Diamantopoulou, A., Raftogianni, A., Stamatakis, A., Alikaridis, F., Oitzl, M. S., & Stylianopoulou, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033793 · Cited by 24
“According to literature, aggressive male rats have a more proactive behavioral response linked to behavioral rigidity, whereas non-aggressive or reactive (submissive) males appear to be more adaptive, responding only when necessary [68,95,96].”
BackgroundAggression and aspects of impulsivity in wild‐type rats
Coppens, C. M., de Boer, S. F., Buwalda, B., & Koolhaas, J. M. (2014) · Aggressive Behavior · doi:10.1002/ab.21527 · Cited by 24
Self-citationHeritability of interpack aggression in a wild pedigreed population of North American grey wolves
vonHoldt, B. M., DeCandia, A. L., Heppenheimer, E., Janowitz‐Koch, I., Shi, R., Zhou, H., German, C. A., Brzeski, K. E., Cassidy, K. A., Stahler, D. R., et al. (2020) · Molecular Ecology · doi:10.1111/mec.15349 · Cited by 22
Anti-aggressive effects of neuropeptide S independent of anxiolysis in male rats
Beiderbeck, D. I., Lukas, M., & Neumann, I. D. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00185 · Cited by 22
“With respect to a possible link between inter-male aggression and anxiety, studies describe either an association between low levels of anxiety and high levels of aggression (Nyberg et al., 2003; Beiderbeck et al., 2007), or no such link (De Boer et al., 2003).”
Neuropeptides as facilitators of domestication
Herbeck, Y. E., & Gulevich, R. G. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2939-2 · Cited by 24
Aggressive behavior in cattle is associated with a polymorphism in the MAOA gene promoter
Eusebi, P. G., Sevane, N., Cortés, O., Contreras, E., Cañon, J., & Dunner, S. (2020) · Animal Genetics · doi:10.1111/age.12867 · Cited by 21
“Accepted for publication 18 September 2019 doi: 10.1111/age.12867 1© 2019 Stichting International Foundation for Animal Genetics aggressiveness (de Boer et al. 2003); however, the molecular mechanisms involved in its initiation and progression are still unknown.”
BackgroundInfluentialInter-individual differences in laboratory rats as revealed by three behavioural tasks
Rudolfová, V., Petrásek, T., Antošová, E., Frynta, D., Landová, E., Valeš, K., & Nekovářová, T. (2022) · Scientific Reports · doi:10.1038/s41598-022-13288-w · Cited by 21
Hammond, A., Rowland, T., Mills, D. S., & Pilot, M. (2022) · Evolutionary Applications · doi:10.1111/eva.13479 · Cited by 23
“…its genetic and neurobiological bases, are all of theoretical interest within the broader context of the evolution of animal behavioural traits (De Boer et al., 2003; Dubois & Giraldeau, 2005; Maynard- Smith & Price, 1973; Nelson & Trainor, 2007), but also of practical importance in the context…”
BackgroundPreclinical models of conduct disorder – principles and pharmacologic perspectives
Haller, J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.032 · Cited by 21
Endogenous opioids regulate glucocorticoid-dependent stress-coping strategies in mice
Szklarczyk, K., Korostyński, M., Gołda, S., Piechota, M., Ficek, J., & Przewłocki, R. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.034 · Cited by 20
“In aggressive and active individuals, like SWR/J mice, the mitigation of stress is principally aimed at prevention or manipulation of a stressor (de Boer et al., 2003).”
BackgroundAggressive behavior in transgenic animal models: A systematic review
Jager, A., Maas, D. A., Fricke, K., de Vries, R. B., Poelmans, G., & Glennon, J. C. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.028 · Cited by 21
Gracceva, G., Koolhaas, J. M., & Groothuis, T. G. G. (2011) · Developmental Psychobiology · doi:10.1002/dev.20586 · Cited by 19
Self-citationSummers, T. R., Summers, T. L., Carpenter, R. E., Smith, J. P., Young, S. L., Meyerink, B. L., Orr, T. Z., Arendt, D. H., & Summers, C. H. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00515 · Cited by 19
“Behavioral and physiological components of coping styles exhibit a moderate to high degree of heritability (Driscoll et al., 1998; Ellenbroek and Cools, 2002; de Boer et al., 2003; Veenema et al., 2003), including in rainbow trout (Oncorhynchus mykiss) (Pottinger and Carrick, 1999).”
Backgroundvan Heukelum, S., Mogavero, F., van de Wal, M. A. E., Geers, F. E., França, A. S. C., Buitelaar, J. K., Beckmann, C. F., Glennon, J. C., & Havenith, M. N. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00809 · Cited by 20
“An attack was defined as a bite directed at the back, belly, neck, or face of an intruder (12, 47).”
BackgroundGender and Personality Differences in Response to Social Stressors in Great Tits (Parus major)
van der Meer, E., & van Oers, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127984 · Cited by 19
Pacheco, X. P. (2020) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-020-02880-7 · Cited by 20
“This dimension shared similarities with the dimension described as proactive in rats (de Boer et al. 2003) and fish (Mesquita et al. 2016; Baker et al. 2018), dominance in rhesus macaques (Weiss et al. 2011), and confidence in rhesus macaques and chimpanzees (Freeman and Gosling 2010), and in sea…”
Kops, M. S., Kjær, J. B., Güntürkün, O., Westphal, K. G. C., Korte-Bouws, G. A. H., Olivier, B., Bolhuis, J. E., & Korte, S. M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.03.050 · Cited by 18
Oxytocin: Coevolution of human and domesticated animals
Herbeck, Y. E., Gulevich, R. G., Shepeleva, D. V., & Grinevich, V. (2017) · Russian Journal of Genetics Applied Research · doi:10.1134/s2079059717030042 · Cited by 18
MARIA, B. D., Bari, V., Sgoifo, A., Carnevali, L., Cairo, B., Vaini, E., Catai, A. M., Takahashi, A. C. D. M., Vecchia, L. A. D., & Porta, A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01478 · Cited by 18
“The relevance of the simultaneous assessment of RRV and QTV is even more evident when the WT rats were subdivided into non-AGG and AGG animals (de Boer et al., 2003).”
BackgroundMultidimensional nature of dominant behavior: Insights from behavioral neuroscience
Murlanova, K., Kirby, M., Libergod, L., Pletnikov, M. V., & Pinhasov, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.015 · Cited by 17
Hiadlovská, Z., Bímová, B. V., Mikula, O., Piálek, J., & Macholán, M. (2012) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2012.01997.x · Cited by 16
“All statistical procedures were performed using R 2.14.0 (R Development Core Team, 2011), with the packages ‘exactRankTests’ (Hothorn & Hornik, 2006) for Wilcoxon rank sum tests and ‘compositions’ (van den Boogaart, Tolosana & Bren, 2011) for the analysis of compositional data.”
BackgroundMethodInfluentialBiologically Inspired Emotional Expressions for Artificial Agents
Korcsok, B., Konok, V., Persa, G., Faragó, T., Niitsuma, M., Miklósi, Á., Köröndi, P., Bárányi, P., & Gácsi, M. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.01191 · Cited by 17
“…grid becomes bigger than sphere Sphere becomes red, grid becomes blue Scott and Fredericson, 1951; Evans and Norris, 1996 Evans and Norris, 1996; de Boer et al., 2003 Dill, 1978; Nishida et al., 1999; de Boer et al., 2003 Scott and Fredericson, 1951; Evans and Norris, 1996; Nishida et al.,…”
BackgroundInfluentialAdriaansen-Tennekes, R., Decuypere, E. M. P., Parmentier, H. K., & Savelkoul, H. F. J. (2009) · Poultry Science · doi:10.3382/ps.2009-00150 · Cited by 15
Aggressive Behavior and Social Stress
de Boer, S. F., Buwalda, B., & Koolhaas, J. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800951-2.00036-4 · Cited by 16
Self-citationCross-species Analyses of Intra-species Behavioral Differences in Mammals and Fish
Demin, K. A., Lakstygal, A. M., Volgin, A. D., de Abreu, M. S., Genário, R., Alpyshov, E. T., Serikuly, N., Wang, D., Wang, J., Yan, D., et al. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2019.12.035 · Cited by 17
Low β2 Main Peak Frequency in the Electroencephalogram Signs Vulnerability to Depression
Claverie, D., Becker, C., Ghestem, A., Coutan, M., Camus, F., Bernard, C., Benoliel, J. J., & Canini, F. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00495 · Cited by 13
“Male wild-type Groningen (WTG) rats weighing 550–600 g (Groningen, Netherlands) were used as resident rats in confrontation encounters (de Boer et al., 2003).”
MethodIndividual differences in chemotherapy-induced anticipatory nausea
Rodríguez, M. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00502 · Cited by 12
“Similarly, the connection between hostility and AN could be studied in animals by using some rat strains that differ in their latency to attack an opponent male—the shorter the latency of attack the higher the supposed level of aggression (e.g., de Boer et al., 2003).”
BackgroundPersonality traits affect learning performance in dwarf goats (Capra hircus)
Finkemeier, M., Krause, A., Tuchscherer, A., Puppe, B., & Langbein, J. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.916459 · Cited by 11
MDMA-induced serotonergic neurotoxicity enhances aggressiveness in low- but not high-aggressive rats
Wallinga, A. E., ten Voorde, A. M., de Boer, S. F., Koolhaas, J. M., & Buwalda, B. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.07.006 · Cited by 10
“Furthermore, they show a wide and consistent individual variation in aggressive behavior, in contrast to other laboratory rat strains where the display and individual variation of aggression is only poorly expressed (de Boer et al., 2003).”
InfluentialSelf-citationTail skin temperatures reflect coping styles in rats
Ågren, G., Lund, I., Thiblin, I., & Lundeberg, T. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.11.003 · Cited by 10
“Variation in coping-style is primarily found in out-bred and wild-type strains [2,10], but could occur in inbred strains as well [11,12].”
Žampachová, B., Landová, E., & Frynta, D. (2017) · Lynx new series · doi:10.2478/lynx-2017-0011 · Cited by 9
Coping Styles and Aggression: A Biobehavioral Approach
Koolhaas, J. M., & de Boer, S. F. (2007) · Springer eBooks · doi:10.1007/978-0-387-29986-0_2 · Cited by 9
“In line with the concept of proactive and reactive coping, this fear can be expressed either as burying behavior or as immobility behavior ( De Boer, Van Der Vegt, & Koolhaas, 2003 ).”
BackgroundSelf-citationOxytocin: co-evolution of human and domesticated animals
Herbeck, Y. E., Gulevich, R. G., Shepeleva, D. V., & Grinevich, V. (2016) · Vavilov Journal of Genetics and Breeding · doi:10.18699/vj16.145 · Cited by 9
Independent effects of early-life experience and trait aggression on cardiovascular function
Rana, S., Pugh, P. C., Katz, E. M., Stringfellow, S. A., Lin, C. P., Wyss, J. M., Stauss, H. M., White, C. R., Clinton, S. M., & Kerman, I. A. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00505.2015 · Cited by 8
“However, these rats are from the tail of the distribution that exhibits the 492 highest levels of aggression with >55% offense (21).”
BackgroundInfluentialMeasuring behavioral coping style and stress reactivity experimentally in wild olive baboons
Pritchard, A. J., & Palombit, R. A. (2021) · Behavioural Processes · doi:10.1016/j.beproc.2021.104564 · Cited by 8
Can laboratory animals violate behavioural norms? Towards a preclinical model of conduct disorder
Macrı̀, S., Zoratto, F., Chiarotti, F., & Giovanni Laviola, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.047 · Cited by 8
Mustika, D., Nishimura, Y., Ueno, S., Tominaga, S., Shimizu, T., Tajiri, N., Jung, C., & Hida, H. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1356189 · Cited by 8
The relationship between different types of genetically defined aggressive behavior
Ilchibaeva, T. V., Tsybko, A. S., Kozhemyakina, R. V., Konoshenko, M. Y., Popova, N. K., & Naumenko, V. S. (2016) · Journal of Ethology · doi:10.1007/s10164-016-0493-5 · Cited by 7
“Agonistic behavior of aggressive and nonaggressive males was assessed according to the following behavioral indicators (de Boer et al. 2003): latency time of the first aggressive interaction, the number of attacks and the duration of each attack, persecution (yes/no), the number of hind limb beats,…”
MethodPritchard, A. J., & Palombit, R. A. (2022) · American Journal of Primatology · doi:10.1002/ajp.23429 · Cited by 7
“This is concordant with the prediction that coping style variation is a grouping of personality traits (Finkemeier et al., 2018), but also reifies associations from traditional coping style theory (de Boer et al., 2003; Koolhaas et al., 1999; Øverli et al., 2004).”
ResultWhen are females dominant over males in rats (Rattus norvegicus)?
Puentes-Escamilla, M. A., Schweinfurth, M. K., & Hemelrijk, C. K. (2024) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-024-03465-4 · Cited by 6
“…rats show higher levels of aggression (in frequency and intensity) than domesticated strains like Wistar and their behaviour resembles that of wild rats more than other laboratory strains because they have not been bred for specific purposes like other strains have been (de Boer et al. 2003).”
Aggression shapes the gut microbiome; a study in rats
Voulgari‐Kokota, A., Salles, J. F., & Schoemaker, R. G. (2024) · PLoS ONE · doi:10.1371/journal.pone.0312423 · Cited by 6
Whitten, C. J., King, J. E., Rodriguez, R. M., Hennon, L. M., Scarborough, M. C., Hooker, M. K., Jenkins, M. S., Katigbak, I. M., & Cooper, M. A. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105577 · Cited by 6
Sleep biomarkers for stress-induced vulnerability to depression
Claverie, D., Becker, C., Ghestem, A., Coutan, M., Bernard, C., Trousselard, M., Benoliel, J. J., & Canini, F. (2023) · SLEEP · doi:10.1093/sleep/zsad068 · Cited by 6
Decreased dendritic spine density in posterodorsal medial amygdala neurons of proactive coping rats
Anilkumar, S., Patel, D., de Boer, S. F., Chattarji, S., & Buwalda, B. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112940 · Cited by 6
Adolescent social defeat disturbs adult aggression-related impulsivity in wild-type rats
Coppens, C. M., Coolen, A., de Boer, S. F., & Koolhaas, J. M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.10.013 · Cited by 6
Self-citationLind, S. F., Stam, F., Zelleroth, S., Frick, A., & Grönbladh, A. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114678 · Cited by 5
“However, the role of caffeine in relation to anxiety is not fully elucidated.”
BackgroundGenetic and Epigenetic Determinants of Aggression
Klausz, B., Haller, J., Tulogdi, Á., & Zelena, D. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3345-3_9 · Cited by 6
Tail posture and motion as a possible indicator of emotional state in pigs
Groffen, J. (2012) · Epsilon Archive for Student Projects (University of Southampton) · Cited by 5
Nishitani, T., Matsumura, K., Postma, E., Sharma, M. D., Hosken, D. J., & Miyatake, T. (2024) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-024-03451-w · Cited by 4
“More aggressive males engage in contests faster or more often (Benus et al. 1991 ; de Boer et al. 2003 ), but the duration of each fight will depend on an individual’s cost threshold – the point at which costs can no longer be met (Taylor and Elwood 2003 ).”
Wildlife Trade, Behaviour and Avian Invasions
Carrete, M., & Tella, J. L. (2016) · Cambridge University Press eBooks · doi:10.1017/cbo9781139939492.019 · Cited by 4
Pritchard, A. J., Carter, A. J., & Palombit, R. A. (2023) · Animal Behaviour · doi:10.1016/j.anbehav.2023.01.011 · Cited by 4
Frýdlová, P., Šimková, O., Janovská, V., Velenský, P., & Frynta, D. (2016) · acta ethologica · doi:10.1007/s10211-016-0246-z · Cited by 4
“…of aggression in adults have been performed on many species, including fishes (Prenter et al. 2008), squamate reptiles (Tokarz 1985), shorebirds (Szekely et al. 2004), mammals (Clutton-Brock et al. 1982; Kojola 1991), and even laboratory rats andmice (de Boer et al. 2003; Miczek et al. 2001).”
BackgroundBiological Evolution of Violence and Aggression. I. Evolution and Genetics
Sturmey, P. (2022) · Springer eBooks · doi:10.1007/978-3-031-04386-4_4 · Cited by 3
Haller, J. (2014) · Springer eBooks · doi:10.1007/978-3-7091-1268-7_2 · Cited by 3
Gene expression profiles underlying aggressive behavior in the prefrontal cortex of cattlePreprint
Eusebi, P. G., Sevane, N., Pizarro, M., Valero, M., & Dunner, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.09.194704 · Cited by 3
“…attempts to mold abnormal forms of aggressiveness using mainly murine models, and to a lesser extent dogs and semi-domesticated species such as the silver fox, have been performed to display a contrast between docile or tame behaviors and escalated levels of aggressiveness (de Boer et al. 2003).”
BackgroundSapronova, A. A., Kisaretova, P. E., Salman, R., & Bondar, N. P. (2023) · Neurochemical Journal · doi:10.1134/s1819712423030169 · Cited by 2
Dominance relations of Norway rats in groups versus pairs
Puentes-Escamilla, M. A., Schweinfurth, M., & Hemelrijk, C. (2025) · Animal Behaviour · doi:10.1016/j.anbehav.2025.123132 · Cited by 2
Towards streamlined bank vole odor preference evaluation using Y-mazes
Engman, M., Schlyter, F., Koteja, P., Birgersson, G., Olsson, G. E., Witzell, J., & Löf, M. (2019) · Mammal Research · doi:10.1007/s13364-019-00445-2 · Cited by 2
Polymorphic Evolutionary Games and Non-Mendelian Genetics
Fishman, M. A. (2020) · Bulletin of Mathematical Biology · doi:10.1007/s11538-020-00705-2 · Cited by 2
Senko, T., Svitok, P., & Kršková, L. (2017) · General Physiology and Biophysics · doi:10.4149/gpb_2017013 · Cited by 2
Normal and Abnormal Aggressions: Definitions and Operational Approaches
Haller, J. (2014) · Springer eBooks · doi:10.1007/978-3-7091-1268-7_1 · Cited by 2
Serotonergic Modulation of Sex and Aggression
Olivier, B., Chan, J. S. W., & Waldinger, M. D. (2008) · Springer eBooks · doi:10.1007/978-3-540-79288-8_3 · Cited by 2
Animal Models of Aggression and Violence
de Boer, S. F., & Koolhaas, J. M. (2017) · The Wiley Handbook of Violence and Aggression · doi:10.1002/9781119057574.whbva021 · Cited by 2
Self-citationWu, X., Lloyd, H., Dong, L., Zhang, Y., & Lyu, N. (2024) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-024-03546-4 · Cited by 1
“…effects may in turn cause personality in captive-reared animals to differ from wild populations, such as reduced aggressive - ness and activity (de Boer et al. 2003), increased boldness (McPhee 2004 ), increased tolerance of conspecifics (Boice 1972) or even a loss of variation in personality…”
Rudolfová, V., Antošová, E., Petrásek, T., Valeš, K., Landová, E., Frynta, D., & Nekovářová, T. (2025) · Behavioural Processes · doi:10.1016/j.beproc.2025.105205 · Cited by 1
Is aggression related to inhibitory control in a free-living female songbird?
van Iersel, R., Pinxten, R., & Eens, M. (2025) · Behavioral Ecology · doi:10.1093/beheco/araf126 · Cited by 1
Cussen, V. A., Lu, Q., & Reid, P. J. (2025) · PLoS ONE · doi:10.1371/journal.pone.0335278 · Cited by 1
Integrative focus on dynamic motor patterns and age hierarchy in the expression of aggression
Nathaniel, T. I., Aremu, M., Femi, O., & Chima, C. I. (2007) · Open Life Sciences · doi:10.2478/s11535-007-0027-9 · Cited by 1
Simpson, S. A. (2017) · Cambridge University Press eBooks · doi:10.1017/9781316556702.004 · Cited by 1
Serotonin in the Nervous System: Few Neurons Regulating Many Functions
Trueta, C., & Cercós, M. G. (2024) · IntechOpen eBooks · doi:10.5772/intechopen.1005385 · Cited by 1
Maned wolves (Chrysocyon brachyurus) differ in their responses to environmental enrichment: Why?
de Brito, L. D. J. M., de Azevedo, C. S., Dutra, L. M. L., Leme, F. D. O. P., & Vasconcellos, A. D. S. (2024) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2024.106432 · Cited by 1
The Role of Emerging Techniques in Understanding Aggression
Haller, J. (2014) · Springer eBooks · doi:10.1007/978-3-7091-1268-7_5 · Cited by 1
Febrile and sleep responses to an immune challenge are affected by trait aggressiveness in rats
Statello, R., Carnevali, L., Bianchi, S., Sgoifo, A., & Imeri, L. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.04.007 · Cited by 1
de Boer, S. F., & Koolhaas, J. M. (2024) · Wiley eBooks · doi:10.1002/9781119555278.ch22 · Cited by 1
Self-citationVarholick, J. A. (2014) · NC Digital Online Collection of Knowledge and Scholarship (The University of North Carolina at Greensboro)
Aggression, impulsive choice and serotonin in male golden hamsters
Cervantes, M. (2010) · Texas ScholarWorks (Texas Digital Library)
Natarajan, D. (2010) · University of Groningen research database (University of Groningen / Centre for Information Technology)
The physiology of aggression: towards understanding violence
Caramaschi, D. (2009) · University of Groningen research database (University of Groningen / Centre for Information Technology)
Adriaansen-Tennekes, R., Decuypere, E. M. P., Parmentier, H. K., & Savelkoul, H. F. J. (2009)
Animal Models of Psychogenic Cardiovascular Disorders
Nalivaiko, E., Carnevali, L., Grippo, A. J., & Sgoifo, A. (2015) · Springer eBooks · doi:10.1007/978-981-4560-53-5_45-1
Behavioural Co-morbidities in Rat Models of Neuropathic Pain
Legg, E. D. (2011) · Spiral (Imperial College London) · doi:10.25560/9070
Metadata
- 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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