Hormone-dependent aggression in male and female rats: Experiential, hormonal, and neural foundations

Albert, D.J.; Jonik, R.H.; Walsh, M.L.

doi:10.1016/s0149-7634(05)80179-4

Cited by 167Neuroendocrine regulation and behaviorSexual Differentiation and DisordersAnimal Behavior and Reproduction

Hormone-dependent aggression in male and female rats: Experiential, hormonal, and neural foundations

Albert, D.J., Jonik, R.H., Walsh, M.L.·1992·Neuroscience & Biobehavioral Reviews

DOI 10.1016/s0149-7634(05)80179-4

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Abstract

Hormone-dependent aggression in both male and female rats includes the distinctive behavioral characteristics of piloerection and lateral attack. In males the aggression is dependent on testicular testosterone and is commonly known as intermale aggression. In females, the aggression is most commonly observed as maternal aggression and is dependent on hormones whose identity is only beginning to emerge. The present review examines the experiential events which activate hormone-dependent aggression, the relation of the aggression to gonadal hormones, and the neural structures that participate in its modulation. In males and females, the aggression is activated by cohabitation with a conspecific of the opposite sex, by competitive experience, and by repeated exposure to unfamiliar conspecifics. In the female, the presence of pups also activates aggression. In both males and females, hormones are necessary for the full manifestation of the aggression. The essential hormone appears to be testosterone in males and a combination of testosterone and estradiol in females. The information available suggests the neural control systems for hormone-dependent aggression may be similar in males and females. It is argued that hormone-dependent aggression is behaviorally and biologically homologous in male and female rats.

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Adult female laboratory rats display aggression mainly during pregnancy and lactation.
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In male rats, fights are generally much more common than in females, but social ranks have been observed also among females.
“In males, fights are generally much more common than in females, but some authors managed to observe social ranks also among the latter.56,94,111,112”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [56]

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Intermale social aggression: Reinstatement in castrated rats by implants of testosterone propionate in the medial hypothalamus
Albert, D. J., Dyson, E. M., & Walsh, M. L. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90153-3 · Cited by 34 · see citing works
Self-citation
Competitive behavior in male rats: Aggression and success enhanced by medial hypothalamic lesions as well as by testosterone implants
Albert, D. J., Dyson, E. M., & Walsh, M. L. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90270-8 · Cited by 33 · see citing works
Self-citation
Activation of aggression in female rats by normal males and by castrated males with testosterone implants
Albert, D. J., Dyson, E. M., Petrovic, D. M., & Walsh, M. L. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90339-3 · Cited by 33 · see citing works
Self-citation
Intermale social aggression in rats: Suppression by medial hypothalamic lesions independently of enhanced defensiveness or decreased testicular testosterone
Albert, D. J., Dyson, E. M., Walsh, M. L., & Gorzalka, B. B. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90252-6 · Cited by 32 · see citing works
Self-citation
Effect of histamine depletion on the circadian amplitude of the sleep-wakefulness cycle
Itowi, N., Yamatodani, A., Kiyono, S., Hiraiwa, M. L., & Wada, H. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90293-w · Cited by 32 · see citing works
Testicular hormones and intermale aggressive behaviour in the presence of a female rat
Taylor, G. T., Haller, J., Rupich, R. C., & Weiss, J. (1984) · Journal of Endocrinology · doi:10.1677/joe.0.1000315 · Cited by 32 · see citing works
Post partum aggression against intruding male conspecifics in sprague-dawley rats
Flannelly, K. J., Flannelly, L., & Lore, R. (1986) · Behavioural Processes · doi:10.1016/0376-6357(86)90090-2 · Cited by 31 · see citing works
Variations in maternal behavior in the rat as a function of sex and gonadal state
Leroy, L., & Krehbiel, D. (1978) · Hormones and Behavior · doi:10.1016/0018-506x(78)90051-x · Cited by 31 · see citing works
Testosterone supports hormone-dependent aggression in female rats
Albert, D. J., Jonik, R. H., Walsh, M. L., & Petrovic, D. M. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90253-9 · Cited by 30 · see citing works
Self-citation
Hormone-dependent aggression in the female rat: Testosterone plus estradiol implants prevent the decline in aggression following ovariectomy
Albert, D. J., Jonik, R. H., & Walsh, M. L. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90300-d · Cited by 30 · see citing works
Self-citation
Postpartum aggression in rats does not influence threshold currents for EBS-induced aggression
Mos, J., Olivier, B., Lammers, J. H. C. M., van der Poel, A. M., Kruk, M. R., & Zethof, T. J. J. (1987) · Brain Research · doi:10.1016/0006-8993(87)91377-1 · Cited by 29 · see citing works
Extinction induced social interaction in rats
Davis, H., & Donenfeld, I. (1967) · Psychonomic Science · doi:10.3758/bf03328475 · Cited by 29 · see citing works
Competitive experience activates testosterone-dependent social aggression toward unfamiliar males
Albert, D. J., Petrovic, D. M., & Walsh, M. L. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90285-0 · Cited by 28 · see citing works
Self-citation
EFFECTS OF AROMATIZABLE ANDROGENS ON AGGRESSIVE BEHAVIOUR AMONG RATS ( RATTUS NORVEGICUS )
Christie, M. H., & Barfield, R. J. (1979) · Journal of Endocrinology · doi:10.1677/joe.0.0830017 · Cited by 28 · see citing works
Hormone-dependent aggression in female rats: Testosterone implants attenuate the decline in aggression following ovariectomy
Albert, D. J., Jonik, R. H., & Walsh, M. L. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90074-e · Cited by 28 · see citing works
Self-citation
Role of habit and androgen level in food-seeking dominance among rats.
Work, M. S., Grossen, N. E., & Rogers, H. R. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0028247 · Cited by 27 · see citing works
Medial accumbens lesions attenuate testosterone-dependent aggression in male rats
Albert, D. J., Petrovic, D. M., Walsh, M. L., & Jonik, R. H. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90342-9 · Cited by 27 · see citing works
Self-citation
PSEUDOPREGNANCY IN THE ALBINO RAT
Slonaker, J. R. (1929) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1929.89.2.406 · Cited by 26 · see citing works
Medial hypothalamic lesions in the rat enhance reactivity and mouse killing but not social aggression
Albert, D. J., & Walsh, M. L. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90195-0 · Cited by 25 · see citing works
Self-citation
Sex-specific interactions between aggressive and sexual behavior in the rat: Effects of testosterone and progesterone
de Jonge, F. H., Eerland, E. M. J., & van de Poll, N. E. (1986) · Hormones and Behavior · doi:10.1016/0018-506x(86)90005-x · Cited by 25 · see citing works
Defensive aggression and testosterone-dependent intermale social aggression are each elicited by food competition
Albert, D. J., Dyson, E. M., Walsh, M. L., & Wong, R. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90093-5 · Cited by 25 · see citing works
Self-citation
Contrôle amygdalien de comportements d'agression chez le rat
Vergnes, M. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90105-0 · Cited by 24 · see citing works
The effects of ethanol on the offense and defensive behaviors of male and female rats during group formation
Blanchard, R. J., Hori, K., Flannelly, K. J., & Blanchard, D. C. (1987) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(87)90534-x · Cited by 23 · see citing works
The effect of estrogen on fetal survival in progesterone-treated ovariectomized rats.
Tamada, H., & Ichikawa, S. (1980) · Endocrinologia Japonica · doi:10.1507/endocrj1954.27.163 · Cited by 23 · see citing works
Central hormonal replacement and home-cage dominance in castrated rats
Bean, N. J., & Conner, R. L. (1978) · Hormones and Behavior · doi:10.1016/0018-506x(78)90061-2 · Cited by 22 · see citing works
Female rats in a competitive situation: Medial hypothalamic lesions increase and ovariectomy decreases success and aggression
Albert, D. J., Petrovic, D. M., & Walsh, M. L. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90007-3 · Cited by 21 · see citing works
Self-citation
Activity, reactivity, and dominance following septal lesions in rats
Gage, F. H., Olton, D. S., & Bolanowski, D. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)92230-7 · Cited by 19 · see citing works
Defensive aggression toward an experimenter: No differences between males and females following septal, medial accumbens, or medial hypothalamic lesions in rats
Albert, D. J., Walsh, M. L., Zalys, C., & Dyson, E. M. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90125-3 · Cited by 19 · see citing works
Self-citation
Aggression by ovariectomized female rats with testosterone implants: Competitive experience activates aggression toward unfamiliar females
Albert, D. J., Jonik, R. H., & Walsh, M. L. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90080-n · Cited by 18 · see citing works
Self-citation
Effets de lésions précoces de l'amygdale sur le développement de l'agressivité interspécifique du rat
Eclancher, F., Schmitt, P., & Karli, P. (1975) · Physiology & Behavior · doi:10.1016/0031-9384(75)90034-7 · Cited by 18 · see citing works
Aggression by a female rat cohabitating with a sterile male: Termination of pseudopregnancy does not abolish aggression
Albert, D. J., Jonik, R. H., Watson, N. V., Moe, I. V., & Walsh, M. L. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90539-z · Cited by 17 · see citing works
Self-citation
Effects of septal lesions on social dominance in rats
Costanzo, D. J., Enloe, L. J., & Hothersall, D. (1977) · Behavioral Biology · doi:10.1016/s0091-6773(77)91041-0 · Cited by 17 · see citing works
Lesions of the region ventral to the anterior septum increase mouse killing and reactivity but not social attack
Albert, D. J., Chew, G. L., Walsh, M. L., Ryan, J. D., & Lee, C. S. Y. (1982) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(82)91667-3 · Cited by 17 · see citing works
Self-citation
Ventromedial tegmental lesions abolish offense without disturbing predation or defense
Adams, D. B. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90150-2 · Cited by 17 · see citing works
The effect of pup presence and intruder behavior on maternal aggression in rats
Flannelly, K. J., & Kemble, E. D. (1987) · Bulletin of the Psychonomic Society · doi:10.3758/bf03330306 · Cited by 16 · see citing works
Effect of estrogen level on food-seeking dominance among male rats.
Work, M. S., & Rogers, H. R. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0032828 · Cited by 15 · see citing works
Applicability of animal models to human aggression.
Dc, B. (1984) · PubMed · Cited by 15 · see citing works
Steroid Hormone Receptors in Brain and Pituitary
Luine, V. N., & McEwen, B. S. (1985) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4684-4832-0_14 · Cited by 14 · see citing works
Female-enhanced aggression in male rats: Effects of genital anesthesia, castration, or preoptic lesions.
Bergvall, Å. H., & Hansen, S. (1990) · Behavioral Neuroscience · doi:10.1037//0735-7044.104.2.348 · Cited by 14 · see citing works
Effects of different housing conditions on intraspecies fighting between male Long-Evans hooded rats
Barr, G. A. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90367-x · Cited by 14 · see citing works
Interactions between simultaneously activated behavioral systems in the rat.
Lammers, J. H. C. M., van der Noordaa, J., Kruk, M. R., Meelis, W., & al, E. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.4.784 · Cited by 13 · see citing works
Castration, androgens, and dominance status in the rat
Stewart, J., & Palfai, T. (1967) · Psychonomic Science · doi:10.3758/bf03331045 · Cited by 13 · see citing works
Pain and aggression reconsidered.
Rj, B. (1984) · PubMed · Cited by 13 · see citing works
Interactions between simultaneously activated behavioral systems in the rat.
Lammers, J. H. C. M., van der Noordaa, J., Kruk, M. R., et al. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.4.784 · Cited by 13 · see citing works
Aggression by ovariectomized female rats: Combined testosterone/estrogen implants support the development of hormone-dependent aggression
Albert, D. J., Jonik, R. H., & Walsh, M. L. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90004-n · Cited by 12 · see citing works
Self-citation
Intermale aggression of subordinate resident long-evans rats
Takahashi, L. K., & Lore, R. (1983) · Behavioural Processes · doi:10.1016/0376-6357(83)90040-2 · Cited by 12 · see citing works
Influence of the estrous cycle on heterosexual aggression in two strains of rats (S3 and WEzob)
Swanson, H. H., van de Poll, N. E., & van Pelt, J. F. (1982) · Hormones and Behavior · doi:10.1016/0018-506x(82)90048-4 · Cited by 11 · see citing works
Female-enhanced aggression in male rats: Effects of genital anesthesia, castration, or preoptic lesions.
Bergvall, Å. H., & Hansen, S. (1990) · Behavioral Neuroscience · doi:10.1037/0735-7044.104.2.348 · Cited by 11 · see citing works
Effects of isolation during development on reactivity and home-cage agonistic behavior in rats
Wahlstrand, K., Knutson, J. F., & Viken, R. J. (1983) · Aggressive Behavior · doi:10.1002/1098-2337(1983)9:1 · Cited by 9 · see citing works
Behavioral study in rats of paired accumbens-lesioned residents and intact intruders
Fernández‐Espejo, E., & Mir, D. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90022-v · Cited by 8 · see citing works
Spontaneous mouse killing rats: Gentling and food deprivation result in killing behavior almost identical to that of rats with medial hypothalamic lesions
Albert, D. J., Walsh, M. L., Siemens, Y., & Louie, H. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90501-9 · Cited by 8 · see citing works
Self-citation
Effects of Androgen Treatment of Full-Grown Puberally Castrated Rats Upon Male Sexual Behavior, Intermale Aggressive Behavior and the Sequential Patterning of Aggressive Interactions
Bermond, B. (1982) · Behaviour · doi:10.1163/156853982x00337 · Cited by 7 · see citing works
Competitive behavior: Intact male rats but not hyperdefensive males with medial hypothalamic lesions share water with females
Albert, D. J., Dyson, E. M., & Walsh, M. L. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90310-6 · Cited by 7 · see citing works
Self-citation
Fighting behavior displayed during the development of a worker—parasite relationship between rats
Masur, J., & da Silva, V. A. (1977) · Behavioral Biology · doi:10.1016/s0091-6773(77)90492-8 · Cited by 6 · see citing works
Work and water intake and the water need of rats during growth of a tumor
Morrison, S. D. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90120-5 · Cited by 5 · see citing works
Decline in testosterone-dependent aggression of male rats following replacement of intact female cagemates with ovariectomized females
Albert, D. J., Petrovic, D. M., Jonik, R. H., & Walsh, M. L. (1990) · Psychobiology · doi:10.3758/bf03327229 · Cited by 4 · see citing works
Self-citation
Aggression among Female Rats over the Estrus Cycle
Hood, K. E. (1981) · Springer eBooks · doi:10.1007/978-94-009-8609-1_19 · Cited by 3 · see citing works
Agonistic behavior between wild and genetically sterile male Norway rats (rattus norvegicus)
Christensen, M. T. (1977) · Aggressive Behavior · doi:10.1002/1098-2337(1977)3:1 · Cited by 1 · see citing works

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Anger is an approach-related affect: Evidence and implications.
Carver, C. S., & Harmon‐Jones, E. (2009) · Psychological Bulletin · doi:10.1037/a0013965 · Cited by 1,757 · see citing works
Androgens, brain, and behavior
Rubinow, D. R., & Schmidt, P. J. (1996) · American Journal of Psychiatry · doi:10.1176/ajp.153.8.974 · Cited by 417 · see citing works
Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain
Kollack‐Walker, S., & Newman, S. W. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00563-k · Cited by 315 · see citing works
Comparing postnatal development of gonadal hormones and associated social behaviors in rats, mice, and humans
Bell, M. R. (2018) · Endocrinology · doi:10.1210/en.2018-00220 · Cited by 308 · see citing works
Sensory, hormonal, and neural control of maternal aggression in laboratory rodents
Lonstein, J. S., & Gammie, S. C. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00087-8 · Cited by 299 · see citing works
“[4] Albert DJ, Jonik RH, Walsh ML.”
BackgroundResultInfluential
The Role of Androgens in Female Vertebrates
Staub, N. L., & Beer, M. D. (1997) · General and Comparative Endocrinology · doi:10.1006/gcen.1997.6962 · Cited by 251 · see citing works
Effects of Implicit Power Motivation on Men's and Women's Implicit Learning and Testosterone Changes After Social Victory or Defeat.
Schultheiss, O. C., Wirth, M. M., Torges, C. M., Pang, J. S., Villacorta, M. A., & Welsh, K. M. (2005) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.88.1.174 · Cited by 248 · see citing works
“Because women may be more sensitive to even slight changes in T (Sherwin, 1988) and elevated T facilitates female aggression (Albert et al., 1992), powermotivated losers may have been more primed than winners for subsequent dominance challenges.”
Background
Effects of affiliation and power motivation arousal on salivary progesterone and testosterone
Schultheiss, O. C., Wirth, M. M., & Stanton, S. J. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.07.005 · Cited by 184 · see citing works
“E-mail address: oschult@umich.edu (O.C. Schultheiss). by species, gender, and context (e.g., Albert et al., 1992; Bernstein et al., 1983; Mazur and Booth, 1998; Wingfield et al., 1990).”
Background
Aggression in humans: What is its biological foundation?
Albert, D. J., Walsh, M. L., & Jonik, R. H. (1993) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80117-4 · Cited by 180 · see citing works
Self-citation
Dominance Hierarchy Influences Adult Neurogenesis in the Dentate Gyrus: Figure 1.
Kozorovitskiy, Y., & Gould, E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0345-04.2004 · Cited by 179 · see citing works
“Both aggression and mating are linked to enhanced levels of testosterone (Taylor et al., 1985; Albert et al., 1992).”
Background
Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles
Gobrogge, K. L., Liu, Y., Jia, X., & Wang, Z. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21364 · Cited by 178 · see citing works
“…aggression represents a very different manipulation of aggressive behavior than the ones previously reported by using other animal models (Albert et al., 1992; Ferris et al., 1997; Delville et al., 1998; DeLeon et al., 2002b; Ferrari et al., 2003; Miczek et al., 2004; Nelson, 2005;…”
Result
Testosterone and aggressiveness.
Giammanco, M., Tabacchi, G., Giammanco, S., Majo, D. D., & Guardia, M. L. (2005) · PubMed · Cited by 175 · see citing works
The hormonal correlates of implicit power motivation
Stanton, S. J., & Schultheiss, O. C. (2009) · Journal of Research in Personality · doi:10.1016/j.jrp.2009.04.001 · Cited by 172 · see citing works
Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles
Wang, Z., Hulihan, T. J., & Insel, T. R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00617-3 · Cited by 169 · see citing works
Chapter 10 Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats
Neumann, I. D. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33011-x · Cited by 169 · see citing works
Maternal defence as an emotional stressor in female rats: correlation of neuroendocrine and behavioural parameters and involvement of brain oxytocin
Neumann, I. D., Toschi, N., Ohl, F., Torner, L., & Krömer, S. A. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01460.x · Cited by 158 · see citing works
“Although a variety of approaches have been taken in order to understand the hormonal (Mayer & Rosenblatt, 1987; Mayer et al., 1990; Albert et al., 1992) and neurobiological (Ferreira et al., 1987; Hansen, 1989; Factor et al., 1990; Kolunie & Stern, 1995; Consiglio & Lucion, 1996; Lonstein et al.,…”
Background
The role of oxytocin in male and female reproductive behavior
Veening, J. G., A, T. R. D. J., Waldinger, M. D., Korte, S. M., & Olivier, B. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.07.045 · Cited by 156 · see citing works
European Journal of Psychotraumatology
Olff, M., & Bindslev, A. (2011) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v2i0.15546 · Cited by 156 · see citing works
The role of the estrogen receptor alpha in the medial amygdala and ventromedial nucleus of the hypothalamus in social recognition, anxiety and aggression.
Spiteri, T., Musatov, S., Ogawa, S., Ribeiro, A., Pfaff, D., & Ǻgmo, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.033 · Cited by 136 · see citing works
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
“Adult females display aggression mainly during the pregnancy and lactation.(56,57) Apart from coitus and care of young they show mainly amicable behavior.”
Background
Basal and dynamic relationships between implicit power motivation and estradiol in women
Stanton, S. J., & Schultheiss, O. C. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.07.002 · Cited by 125 · see citing works
“Moreover, in humans, aggressive behavior may reflect defensiveness and not dominance, and it is notable that in animals, defensive aggression is not dependent on circulating levels of gonadal steroids whereas dominant aggression is (cf. Albert et al., 1992; Schultheiss and Wirth, in press).”
Background
Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii)
Nunes, S., Fite, J. E., & French, J. A. (2000) · Animal Behaviour · doi:10.1006/anbe.2000.1524 · Cited by 125 · see citing works
The hypothalamus: cross-roads of endocrine and behavioural regulation in grooming and aggression
Kruk, M. R., Westphal, K. G. C., van Erp, A. M. M., van Asperen, J., Cave, B. J., Slater, E., de Koning, J., & Haller, J. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00018-9 · Cited by 123 · see citing works
Brain mechanisms underlying emotional alterations in the peripartum period in rats
Neumann, I. D. (2003) · Depression and Anxiety · doi:10.1002/da.10070 · Cited by 121 · see citing works
Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat.
Frank, E., Salchner, P., Aldag, J. M., Salomé, N., Singewald, N., Landgraf, R., & Wigger, A. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.60 · Cited by 114 · see citing works
Progesterone receptors mediate male aggression toward infants
Schneider, J. S., Stone, M. K., Wynne‐Edwards, K. E., Horton, T. H., Lydon, J. P., O’Malley, B. W., & Levine, J. E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0130100100 · Cited by 113 · see citing works
Increased dopaminergic and 5‐hydroxytryptaminergic activities in male rat brain following long‐term treatment with anabolic androgenic steroids
Thiblin, I., Finn, A., Ross, S. B., & Stenfors, C. (1999) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0702412 · Cited by 108 · see citing works
“Increased aggressive behaviour in animals as a result of AAS administration is well established (Bonson et al., 1994; Albert et al., 1992; Lumia et al., 1994).”
Background
Stress and Reproductive Hormones in Grizzly Bears Reflect Nutritional Benefits and Social Consequences of a Salmon Foraging Niche
Bryan, H. M., Darimont, C. T., Paquet, P. C., Wynne‐Edwards, K. E., & Smits, J. E. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080537 · Cited by 107 · see citing works
“Though usually considered with respect to reproductive traits in males, testosterone in females has been linked with defending resources and acquiring food [87,88].”
Background
Individual differences in estrogen receptor α in select brain nuclei are associated with individual differences in aggression
Trainor, B. C., Greiwe, K. M., & Nelson, R. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.04.002 · Cited by 106 · see citing works
“, 2000) and lesion (Albert et al., 1992) studies that suggest that the AHA, but not the MPOA, modulates aggressive behavior.”
Social hierarchy position in female mice is associated with plasma corticosterone levels and hypothalamic gene expression
Williamson, C. M., Lee, W., DeCasien, A. R., Lanham, A., Romeo, R. D., & Curley, J. P. (2019) · Scientific Reports · doi:10.1038/s41598-019-43747-w · Cited by 99 · see citing works
Hormonal Basis of Social Conflict and Communication
Albers, H. E., Huhman, K. L., & Meisel, R. L. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50008-1 · Cited by 105 · see citing works
Vocal Tract Length Perception and the Evolution of Language
Fitch, W. T., & Fitch, S. (1994) · Cited by 99 · see citing works
Heavily hunted wolves have higher stress and reproductive steroids than wolves with lower hunting pressure
Bryan, H. M., Smits, J. E. G., Koren, L., Paquet, P. C., Wynne‐Edwards, K. E., & Musiani, M. (2014) · Functional Ecology · doi:10.1111/1365-2435.12354 · Cited by 97 · see citing works
Functional Connectivity among Limbic Brain Areas: Differential Effects of Incubation Temperature and Gonadal Sex in the Leopard Gecko, <i>Eublepharis macularius</i>
Sakata, J. T., Coomber, P., Gonzalez-Lima, F., & Crews, D. (2000) · Brain Behavior and Evolution · doi:10.1159/000006648 · Cited by 96 · see citing works
“Such a prediction is very plausible as both the AH and SEP have been implicated in the display of aggression in a number of species [reviewed in Albert et al., 1992; KollackWalker and Newman, 1995; Ferris et al., 1997; Goodson et al., 1999].”
Background
Aggression is related to frontal serotonin‐1A receptor distribution as revealed by PET in healthy subjects
Witte, A. V., Flöel, A., Stein, P., Savli, M., Mien, L., Wadsak, W., Spindelegger, C., Moser, U., Fink, M., Hahn, A., et al. (2008) · Human Brain Mapping · doi:10.1002/hbm.20687 · Cited by 96 · see citing works
“For example, levels of both estrogens and testosterone have been shown to control maternal aggression, whereas primarily testosterone exerts regulatory influence on intermale aggression in rats [reviewed in Albert et al., 1992; Lonstein and Gammie, 2002].”
Background
Serotonergic control of androgen-induced dominance
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Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons
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The Neural Mechanisms of Sexually Dimorphic Aggressive Behaviors
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Sex differences in adult zebrafish anxiolytic-like responses to diazepam and melatonin
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Behavioral correlates of differences in neural metabolic capacity
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Chapter 10 Biopsychological and Neural Processes of Implicit Motivation
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“Animal studies show that testosterone lowers the threshold for aggressive behavior in males and females (Albert et al., 1992), and research conducted in our laboratory suggests that a priming role of testosterone on female assertiveness also exists in humans (Schultheiss et al., 2005).”
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Association between a dinucleotide repeat polymorphism of the estrogen receptor alpha gene and personality traits in women
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Genetics of testosterone and the aggression-hostility-anger (AHA) syndrome: a study of middle-aged male twins
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“A hypothalamic network centered on the anterior nucleus (AN) of the hypothalamus plays a critical role in lateral attack and piloerection and thereby in rats' dominance behavior (Albert et al., 1992; see also Delville, DeVries, & Ferris, 2000).”
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“, 2002; Rosvall, 2013), mammals (Albert et al., 1992; Razzoli et al., 2003), reptiles (Rubenstein and Wikelski, 2005; Woodley and Moore, 1999), and fish (Desjardins et al.”
Brain aromatase activity and plasma testosterone levels are elevated in aggressive male mice during early ontogeny
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Principles for developing animal models of military PTSD
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Genetic differences in female house mice in aggressive response to sex steroid hormone treatment
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“Adult pTc has been put forward as a possible physiological intermediate between the Y chromosome and intermale aggression (Schuurman, 1980; van Oortmerssen et al., 1987; Albert et al., 1992; Zielinski and Vandenbergh, 1993).”
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Neural mechanisms of persistent aggression
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Maternal Aggression
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“Since our animals were reared after weaning separated by sex in groups of 3–5 per cage, males and females had different rearing conditions once male rats are known to present intermale aggression, which is dependent of testosterone and also on experience (Albert et al., 1992).”
Background
Progesterone and maternal aggressive behavior in rats
de Sousa, F. L., Lazzari, V. M., de Azevedo, M. S., Almeida, S., Sanvitto, G. L., Lucion, A. B., & Giovenardi, M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.050 · Cited by 22 · see citing works
Aggression frequency and intensity, independent of testosterone levels, relate to neural activation within the dorsolateral subdivision of the ventromedial hypothalamus in the tree lizard Urosaurus ornatus
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“, 2000), is involved in nPower (see Schultheiss, 2013, for a review) and that nPower thus has many of the hallmarks of power/dominance motivation as studied by biopsychologists and neuroscientists (e.g., Sapolsky, 1987; Albert et al., 1992; Johnson et al., 2012).”
BackgroundInfluential
Ostracism and Aggression among Chinese Adolescents: a Moderated Mediation Model of Trait Anger and Forgiveness
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“adulthood, including salt appetite (53), aggression (54), and pituitary functions (55 , 56).”
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Food availability affects behavior but not circulating gonadal hormones in maternal Belding's ground squirrels
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mGluR5 Mediates Dihydrotestosterone-Induced Nucleus Accumbens Structural Plasticity, but Not Conditioned Reward
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Sensory, Hormonal, and Neural Basis of Maternal Aggression in Rodents
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Female Reproductive Behavior
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Inter-male aggression with regard to polygynous mating system in Pampean grassland mouse, Akodon azarae (Cricetidae: Sigmodontinae)
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“Intruders with different housing conditions than residents could increase their likelihood of being defeated by residents (Valzelli 1973; Barnett 1975; Albert et al. 1992; Kaliste-Korhonen and Eskola 2000; Matsumoto et al. 2005; Bartolomucci et al. 2009; Kraak 2012).”
Background

Hormone-dependent aggression in the female rat: Testosterone plus estradiol implants prevent the decline in aggression following ovariectomy
Albert, D. J., Jonik, R. H., & Walsh, M. L. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90300-d · Cited by 30 · see citing works
Self-citation
Hormone-dependent aggression in male rats is proportional to serum testosterone concentration but sexual behavior is not
Albert, D. J., Jonik, R. H., Watson, N. V., Gorzalka, B. B., & Walsh, M. L. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90336-3 · Cited by 65 · see citing works
Self-citation
Testosterone supports hormone-dependent aggression in female rats
Albert, D. J., Jonik, R. H., Walsh, M. L., & Petrovic, D. M. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90253-9 · Cited by 30 · see citing works
Self-citation
Hormone-dependent aggression in female rats: Testosterone implants attenuate the decline in aggression following ovariectomy
Albert, D. J., Jonik, R. H., & Walsh, M. L. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90074-e · Cited by 28 · see citing works
Self-citation
Hormonal Pathways Regulating Intermale And Interfemale Aggression
Simon, N. G., Mo, Q., Hu, S., Garippa, C., & Lu, S. (2006) · International review of neurobiology · doi:10.1016/s0074-7742(06)73003-3 · Cited by 11 · see citing works

Authors: Albert, D. J., Jonik, R. H., & Walsh, M. L.
Affiliations: University of British Columbia (CA)
ORCID: Albert, D.J.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 1992-06
Volume: 16
Issue: 2
Pages: 177-192
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/s0149-7634(05)80179-4
OpenAlex: W1970628628
Cited by: 167
References: 151
Citations by year: 2026: 1 · 2025: 2 · 2024: 2 · 2023: 16 · 2022: 3 · 2021: 3 · 2020: 1 · 2019: 4 · 2018: 8 · 2017: 1 · 2016: 3 · 2015: 3 · 2014: 8 · 2013: 8 · 2012: 8
FWCI: 12.36
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: Natural Sciences and Engineering Research Council of Canada
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: sex differences in aggression, male-male aggression, maternal aggression, testosterone, estradiol, gonadal hormones, piloerection, rats
MeSH terms: Aggression, Animals, Female, Hormones, Male, Neurons, Rats

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Hormone-dependent aggression in male and female rats: Experiential, hormonal, and neural foundations

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