Abstract
Aggression is a social behavior essential for securing resources and defending oneself and family. Thanks to its indispensable function in competition and thus survival, aggression exists widely across animal species, including humans. Classical works from Tinbergen and Lorenz concluded that instinctive behaviors including aggression are mediated by hardwired brain circuitries that specialize in processing certain sensory inputs to trigger stereotyped motor outputs. They further suggest that instinctive behaviors are influenced by an animal’s internal state and past experiences. Following this conceptual framework, here we review our current understanding regarding the neural substrates underlying aggression generation, highlighting an evolutionarily conserved ‘core aggression circuit’ composed of four subcortical regions. We further discuss the neural mechanisms that support changes in aggression based on the animal’s internal state. We aim to provide an overview of features of aggression and the relevant neural substrates across species, highlighting findings in rodents, primates and songbirds.
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References
Lorenz, K. On Aggression. (Routledge, 2005).
Tinbergen, N. The Study of Instinct (Oxford Univ. Press, 1951).
Allen, J. J., Anderson, C. A. & Bushman, B. J. The general aggression model. Curr. Opin. Psychol. 19, 75–80 (2018).
Dulac, C. & Torello, A. T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci. 4, 551–562 (2003).
Hashikawa, K., Hashikawa, Y., Falkner, A. & Lin, D. The neural circuits of mating and fighting in male mice. Curr. Opin. Neurobiol. 38, 27–37 (2016).
Keshavarzi, S., Power, J. M., Albers, E. H., Sullivan, R. K. & Sah, P. Dendritic organization of olfactory inputs to medial amygdala neurons. J. Neurosci. 35, 13020–13028 (2015).
Caro, S. P., Balthazart, J. & Bonadonna, F. The perfume of reproduction in birds: chemosignaling in avian social life. Horm. Behav. 68, 25–42 (2015).
Stoddard, P. K., Beecher, M. D., Horning, C. L. & Campbell, S. E. Recognition of individual neighbors by song in the song sparrow, a species with song repertoires. Behav. Ecol. Sociobiol. 29, 211–215 (1991).
Searcy, W. A., Anderson, R. C. & Nowicki, S. Bird song as a signal of aggressive intent. Behav. Ecol. Sociobiol. 60, 234–241 (2006).
Theunissen, F. E. & Shaevitz, S. S. Auditory processing of vocal sounds in birds. Curr. Opin. Neurobiol. 16, 400–407 (2006).
Durand, S. E., Tepper, J. M. & Cheng, M. F. The shell region of the nucleus ovoidalis: a subdivision of the avian auditory thalamus. J. Comp. Neurol. 323, 495–518 (1992).
Cheng, M., Chaiken, M., Zuo, M. & Miller, H. Nucleus taenia of the amygdala of birds: anatomical and functional studies in ring doves (Streptopelia risoria) and European starlings (Sturnus vulgaris). Brain Behav. Evol. 53, 243–270 (1999).
Wild, J. M. The ventromedial hypothalamic nucleus in the zebra finch (Taeniopygia guttata): afferent and efferent projections in relation to the control of reproductive behavior. J. Comp. Neurol. 525, 2657–2676 (2017).
Newman, S. W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. NY Acad. Sci. 877, 242–257 (1999).
Goodson, J. L. The vertebrate social behavior network: evolutionary themes and variations. Horm. Behav. 48, 11–22 (2005).
Lischinsky, J. E. et al. Embryonic transcription factor expression in mice predicts medial amygdala neuronal identity and sex-specific responses to innate behavioral cues. eLife 6, e21012 (2017).
Hong, W., Kim, D.-W. & Anderson, D. J. Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell 158, 1348–1361 (2014).
Unger, E. K. et al. Medial amygdalar aromatase neurons regulate aggression in both sexes. Cell Rep. 10, 453–462 (2015).
Padilla, S. L. et al. Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state. Nat. Neurosci. 19, 734–741 (2016).
Goodson, J. L., Evans, A. K. & Soma, K. K. Neural responses to aggressive challenge correlate with behavior in nonbreeding sparrows. Neuroreport 16, 1719–1723 (2005).
Goodson, J. L., Evans, A. K., Lindberg, L. & Allen, C. D. Neuro-evolutionary patterning of sociality. Proc. Biol. Sci. 272, 227–235 (2005).
Meunier, M., Bachevalier, J., Murray, E. A., Málková, L. & Mishkin, M. Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys. Eur. J. Neurosci. 11, 4403–4418 (1999).
Coccaro, E. F., McCloskey, M. S., Fitzgerald, D. A. & Phan, K. L. Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol. Psychiatry 62, 168–178 (2007).
Dong, H.-W., Petrovich, G. D. & Swanson, L. W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 38, 192–246 (2001).
Bayless, D. W. et al. Limbic neurons shape sex recognition and social behavior in sexually naive males. Cell 176, 1190–1205.e20 (2019).
Hashikawa, Y., Hashikawa, K., Falkner, A. L. & Lin, D. Ventromedial hypothalamus and the generation of aggression. Front. Syst. Neurosci. 11, 94 (2017).
Pardo-Bellver, C., Cádiz-Moretti, B., Novejarque, A., Martínez-García, F. & Lanuza, E. Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice. Front. Neuroanat. 6, 33 (2012).
Dong, H. W. & Swanson, L. W. Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J. Comp. Neurol. 471, 396–433 (2004).
Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221–226 (2011).
Lee, H. et al. Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus. Nature 509, 627–632 (2014).
Falkner, A. L., Grosenick, L., Davidson, T. J., Deisseroth, K. & Lin, D. Hypothalamic control of male aggression-seeking behavior. Nat. Neurosci. 19, 596–604 (2016).
Hashikawa, K. et al. Esr1+ cells in the ventromedial hypothalamus control female aggression. Nat. Neurosci. 20, 1580–1590 (2017).
Yang, T. et al. Social control of hypothalamus-mediated male aggression. Neuron 95, 955–970.e4 (2017).
Yang, C. F. et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153, 896–909 (2013).
Remedios, R. et al. Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex. Nature 550, 388–392 (2017).
Falkner, A. L., Dollar, P., Perona, P., Anderson, D. J. & Lin, D. Decoding ventromedial hypothalamic neural activity during male mouse aggression. J. Neurosci. 34, 5971–5984 (2014).
Wang, L. et al. Hypothalamic control of conspecific self-defense. Cell Rep. 26, 1747–1758.e5 (2019).
Kim, D.-W. et al. Multimodal analysis of cell types in a hypothalamic node controlling social behavior. Cell 179, 713–728.e17 (2019).
Putkonen, P. T. Attack elicited by forebrain and hypothalamic stimulation in the chicken. Experientia 22, 405–407 (1966).
Lipp, H. P. & Hunsperger, R. Threat, attack and flight elicited by electrical stimulation of the ventromedial hypothalamus of the marmoset monkey Callithrix jacchus. Brain Behav. Evol. 15, 276–293 (1978).
Siegel, A. & Pott, C. B. Neural substrates of aggression and flight in the cat. Prog. Neurobiol. 31, 261–283 (1988).
Roberts, W. W., Steinberg, M. L. & Means, L. W. Hypothalamic mechanisms for sexual, aggressive, and other motivational behaviors in the opossium, Didelphis virginiana. J. Comp. Physiol. Psychol. 64, 1–15 (1967).
Barbosa, D. A. N. et al. The hypothalamus at the crossroads of psychopathology and neurosurgery. Neurosurg. Focus 43, E15 (2017).
Motta, S. C. et al. Ventral premammillary nucleus as a critical sensory relay to the maternal aggression network. Proc. Natl Acad. Sci. USA 110, 14438–14443 (2013).
Soden, M. E. et al. Genetic isolation of hypothalamic neurons that regulate context-specific male social behavior. Cell Rep. 16, 304–313 (2016).
Stagkourakis, S. et al. A neural network for intermale aggression to establish social hierarchy. Nat. Neurosci. 21, 834–842 (2018).
Kang, S. W., Thayananuphat, A., Bakken, T. & El Halawani, M. E. Dopamine-melatonin neurons in the avian hypothalamus controlling seasonal reproduction. Neuroscience 150, 223–233 (2007).
Lo, L. et al. Connectional architecture of a mouse hypothalamic circuit node controlling social behavior. Proc. Natl Acad. Sci. USA 116, 7503–7512 (2019).
Hashikawa, K., Hashikawa, Y., Lischinsky, J. & Lin, D. The neural mechanisms of sexually dimorphic aggressive behaviors. Trends Genet. 34, 755–776 (2018).
Cameron, A. A., Khan, I. A., Westlund, K. N. & Willis, W. D. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. II. Descending projections. J. Comp. Neurol. 351, 585–601 (1995).
Falkner, A. L. et al. Hierarchical representations of aggression in a hypothalamic-midbrain circuit. Neuron 106, 637–648.e6 (2020).
Tschida, K. et al. A specialized neural circuit gates social vocalizations in the mouse. Neuron 103, 459–472.e4 (2019).
Jürgens, U. & Ploog, D. Cerebral representation of vocalization in the squirrel monkey. Exp. Brain Res. 10, 532–554 (1970).
Golden, S. A., Jin, M. & Shaham, Y. Animal models of (or for) aggression reward, addiction, and relapse: behavior and circuits. J. Neurosci. 39, 3996–4008 (2019).
Couppis, M. H. & Kennedy, C. H. The rewarding effect of aggression is reduced by nucleus accumbens dopamine receptor antagonism in mice. Psychopharmacol. (Berl.) 197, 449–456 (2008).
Golden, S. A. et al. Nucleus accumbens Drd1-expressing neurons control aggression self-administration and aggression seeking in mice. J. Neurosci. 39, 2482–2496 (2019).
Fang, Y.-Y., Yamaguchi, T., Song, S. C., Tritsch, N. X. & Lin, D. A hypothalamic midbrain pathway essential for driving maternal behaviors. Neuron 98, 192–207.e10 (2018).
Nieder, A. & Mooney, R. The neurobiology of innate, volitional and learned vocalizations in mammals and birds. Philos. Trans. R. Soc. Lond. B 375, 20190054 (2020).
Berk, M. L. & Butler, A. B. Efferent projections of the medial preoptic nucleus and medial hypothalamus in the pigeon. J. Comp. Neurol. 203, 379–399 (1981).
Riters, L. V. & Alger, S. J. Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song. Cell Tissue Res. 316, 35–44 (2004).
Lewis, J. W., Ryan, S. M., Arnold, A. P. & Butcher, L. L. Evidence for a catecholaminergic projection to Area X in the zebra finch. J. Comp. Neurol. 196, 347–354 (1981).
Appeltants, D., Absil, P., Balthazart, J. & Ball, G. F. Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Chem. Neuroanat. 18, 117–133 (2000).
Appeltants, D., Ball, G. F. & Balthazart, J. The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 13, 649–653 (2002).
Maney, D. L. & Ball, G. F. Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J. Neurobiol. 56, 163–170 (2003).
Sasaki, A., Sotnikova, T. D., Gainetdinov, R. R. & Jarvis, E. D. Social context-dependent singing-regulated dopamine. J. Neurosci. 26, 9010–9014 (2006).
Yanagihara, S. & Hessler, N. A. Modulation of singing-related activity in the songbird ventral tegmental area by social context. Eur. J. Neurosci. 24, 3619–3627 (2006).
Hara, E., Kubikova, L., Hessler, N. A. & Jarvis, E. D. Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur. J. Neurosci. 25, 3406–3416 (2007).
Tanaka, M., Sun, F., Li, Y. & Mooney, R. A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour. Nature 563, 117–120 (2018).
Glimcher, P. W. Understanding dopamine and reinforcement learning: the dopamine reward prediction error hypothesis. Proc. Natl Acad. Sci. USA 108, 15647–15654 (2011).
Yamaguchi, T. & Lin, D. Functions of medial hypothalamic and mesolimbic dopamine circuitries in aggression. Curr. Opin. Behav. Sci. 24, 104–112 (2018).
van Erp, A. M. & Miczek, K. A. Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J. Neurosci. 20, 9320–9325 (2000).
Aleyasin, H. et al. Cell-type-specific role of ΔFosB in nucleus accumbens in modulating intermale aggression. J. Neurosci. 38, 5913–5924 (2018).
Golden, S. A. et al. Basal forebrain projections to the lateral habenula modulate aggression reward. Nature 534, 688–692 (2016).
Christoph, G. R., Leonzio, R. J. & Wilcox, K. S. Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J. Neurosci. 6, 613–619 (1986).
Russo, S. J. et al. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33, 267–276 (2010).
Shen, W., Flajolet, M., Greengard, P. & Surmeier, D. J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848–851 (2008).
Becker, E. A. & Marler, C. A. Postcontest blockade of dopamine receptors inhibits development of the winner effect in the California mouse (Peromyscus californicus). Behav. Neurosci. 129, 205–213 (2015).
Sokolov, B. P. & Cadet, J. L. Methamphetamine causes alterations in the MAP kinase-related pathways in the brains of mice that display increased aggressiveness. Neuropsychopharmacology 31, 956–966 (2006).
Moore, I. T., Hernandez, J. & Goymann, W. Who rises to the challenge? Testing the challenge hypothesis in fish, amphibians, reptiles, and mammals. Horm. Behav. 123, 104537 (2020).
Fokidis, H. B., Prior, N. H. & Soma, K. K. Fasting increases aggression and differentially modulates local and systemic steroid levels in male zebra finches. Endocrinology 154, 4328–4339 (2013).
Janson, C. & Vogel, E. Hunger and aggression in capuchin monkeys. in Feeding Ecology in Apes and Other Primates (eds. Hohmann, G., Robbins, M. M. & Boesch, C.) 285–312 (Cambridge Univ. Press, 2006).
Rohles, F. H. Jr. & Wilson, L. M. Hunger as a catalyst in aggression. Behaviour 48, 123–130 (1974).
Berthoud, H.-R. Multiple neural systems controlling food intake and body weight. Neurosci. Biobehav. Rev. 26, 393–428 (2002).
Donato, J. Jr. & Elias, C. F. The ventral premammillary nucleus links metabolic cues and reproduction. Front. Endocrinol. (Lausanne) 2, 57 (2011).
Yanagida, H. et al. Effects of ghrelin on neuronal activity in the ventromedial nucleus of the hypothalamus in infantile rats: an in vitro study. Peptides 29, 912–918 (2008).
Oomura, Y. & Kita, H. Insulin acting as a modulator of feeding through the hypothalamus. Diabetologia 20 Suppl., 290–298 (1981).
Vestlund, J. et al. Ghrelin and aggressive behaviours-evidence from preclinical and human genetic studies. Psychoneuroendocrinology 104, 80–88 (2019).
He, Y. et al. Estrogen receptor-α expressing neurons in the ventrolateral VMH regulate glucose balance. Nat. Commun. 11, 2165 (2020).
Todd, W. D. et al. A hypothalamic circuit for the circadian control of aggression. Nat. Neurosci. 21, 717–724 (2018).
Bliwise, D. L. What is sundowning? J. Am. Geriatr. Soc. 42, 1009–1011 (1994).
Goodson, J. L. Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen. Comp. Endocrinol. 111, 233–244 (1998).
Goodson, J. L., Kelly, A. M., Kingsbury, M. A. & Thompson, R. R. An aggression-specific cell type in the anterior hypothalamus of finches. Proc. Natl Acad. Sci. USA 109, 13847–13852 (2012).
Wingfield, J. C., Hegner, R. E., Dufty, A. M. Jr. & Ball, G. F. The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136, 829–846 (1990).
Xu, X. et al. Modular genetic control of sexually dimorphic behaviors. Cell 148, 596–607 (2012).
Tramontin, A. D., Wingfield, J. C. & Brenowitz, E. A. Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J. Neurobiol. 57, 130–140 (2003).
Soma, K. K., Tramontin, A. D., Featherstone, J. & Brenowitz, E. A. Estrogen contributes to seasonal plasticity of the adult avian song control system. J. Neurobiol. 58, 413–422 (2004).
Bard, P. A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am. J. Physiol. 84, 490–515 (1928).
Paxinos, G. & Franklin, K.B. The Mouse Brain in Stereotaxic Coordinates (Academic Press, 2019).
Anderson, S. W., Bechara, A., Damasio, H., Tranel, D. & Damasio, A. R. Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat. Neurosci. 2, 1032–1037 (1999).
Damasio, H., Grabowski, T., Frank, R., Galaburda, A. M. & Damasio, A. R. The return of Phineas Gage: clues about the brain from the skull of a famous patient. Science 264, 1102–1105 (1994).
Best, M., Williams, J. M. & Coccaro, E. F. Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder. Proc. Natl Acad. Sci. USA 99, 8448–8453 (2002).
Soloff, P. H. et al. Impulsivity and prefrontal hypometabolism in borderline personality disorder. Psychiatry Res. 123, 153–163 (2003).
Molero-Chamizo, A., Martín Riquel, R., Moriana, J. A., Nitsche, M. A. & Rivera-Urbina, G. N. Bilateral prefrontal cortex anodal tDCS effects on self-reported aggressiveness in imprisoned violent offenders. Neuroscience 397, 31–40 (2019).
Pietrini, P., Guazzelli, M., Basso, G., Jaffe, K. & Grafman, J. Neural correlates of imaginal aggressive behavior assessed by positron emission tomography in healthy subjects. Am. J. Psychiatry 157, 1772–1781 (2000).
Ochsner, K. N., Bunge, S. A., Gross, J. J. & Gabrieli, J. D. Rethinking feelings: an fMRI study of the cognitive regulation of emotion. J. Cogn. Neurosci. 14, 1215–1229 (2002).
Mann, J. J. Neurobiology of suicidal behaviour. Nat. Rev. Neurosci. 4, 819–828 (2003).
Soloff, P. H., Meltzer, C. C., Greer, P. J., Constantine, D. & Kelly, T. M. A fenfluramine-activated FDG-PET study of borderline personality disorder. Biol. Psychiatry 47, 540–547 (2000).
Takahashi, A., Nagayasu, K., Nishitani, N., Kaneko, S. & Koide, T. Control of intermale aggression by medial prefrontal cortex activation in the mouse. PLoS One 9, e94657 (2014).
Biro, L. et al. Task division within the prefrontal cortex: distinct neuron populations selectively control different aspects of aggressive behavior via the hypothalamus. J. Neurosci. 38, 4065–4075 (2018).
Caramaschi, D., de Boer, S. F., de Vries, H. & Koolhaas, J. M. Development of violence in mice through repeated victory along with changes in prefrontal cortex neurochemistry. Behav. Brain Res. 189, 263–272 (2008).
Centenaro, L. A. et al. Social instigation and aggressive behavior in mice: role of 5-HT1A and 5-HT1B receptors in the prefrontal cortex. Psychopharmacol. (Berl.) 201, 237–248 (2008).
Veiga, C. P., Miczek, K. A., Lucion, A. B. & Almeida, R. M. Effect of 5-HT1B receptor agonists injected into the prefrontal cortex on maternal aggression in rats. Braz. J. Med. Biol. Res. 40, 825–830 (2007).
Alexander, W. H. & Brown, J. W. Medial prefrontal cortex as an action-outcome predictor. Nat. Neurosci. 14, 1338–1344 (2011).
Harenski, C. L., Harenski, K. A., Shane, M. S. & Kiehl, K. A. Aberrant neural processing of moral violations in criminal psychopaths. J. Abnorm. Psychol. 119, 863–874 (2010).
Kingsbury, L. et al. Correlated neural activity and encoding of behavior across brains of socially interacting animals. Cell 178, 429–446.e16 (2019).
So, N., Franks, B., Lim, S. & Curley, J. P. A social network approach reveals associations between mouse social dominance and brain gene expression. PLoS One 10, e0134509 (2015).
Zhou, T. et al. History of winning remodels thalamo-PFC circuit to reinforce social dominance. Science 357, 162–168 (2017).
Wang, F. et al. Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science 334, 693–697 (2011).
Vertes, R. P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51, 32–58 (2004).
Ongür, D., An, X. & Price, J. L. Prefrontal cortical projections to the hypothalamus in macaque monkeys. J. Comp. Neurol. 401, 480–505 (1998).
Freedman, L. J., Insel, T. R. & Smith, Y. Subcortical projections of area 25 (subgenual cortex) of the macaque monkey. J. Comp. Neurol. 421, 172–188 (2000).
Hardy, S. G. & Leichnetz, G. R. Frontal cortical projections to the periaqueductal gray in the rat: a retrograde and orthograde horseradish peroxidase study. Neurosci. Lett. 23, 13–17 (1981).
An, X., Bandler, R., Ongür, D. & Price, J. L. Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J. Comp. Neurol. 401, 455–479 (1998).
Franklin, T. B. et al. Prefrontal cortical control of a brainstem social behavior circuit. Nat. Neurosci. 20, 260–270 (2017).
Wong, L. C. et al. Effective modulation of male aggression through lateral septum to medial hypothalamus projection. Curr. Biol. 26, 593–604 (2016).
Albert, D. J. & Chew, G. L. The septal forebrain and the inhibitory modulation of attack and defense in the rat. A review. Behav. Neural Biol. 30, 357–388 (1980).
Goodson, J., Eibach, R., Sakata, J. & Adkins-Regan, E. Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla). Behav. Brain Res. 98, 167–180 (1998).
Risold, P. Y. & Swanson, L. W. Connections of the rat lateral septal complex. Brain Res. Brain Res. Rev. 24, 115–195 (1997).
Leroy, F. et al. A circuit from hippocampal CA2 to lateral septum disinhibits social aggression. Nature 564, 213–218 (2018).
Hitti, F. L. & Siegelbaum, S. A. The hippocampal CA2 region is essential for social memory. Nature 508, 88–92 (2014).
Sheehan, T. P., Chambers, R. A. & Russell, D. S. Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res. Brain Res. Rev. 46, 71–117 (2004).
Scott, J. P. Agonistic behavior of mice and rats: a review. Am. Zool. 6, 683–701 (1966).
Maney, D. L. & Goodson, J. L. Neurogenomic mechanisms of aggression in songbirds. Adv. Genet. 75, 83–119 (2011).
Conner, K. R., Duberstein, P. R., Conwell, Y. & Caine, E. D. Reactive aggression and suicide: theory and evidence. Aggress. Violent Behav. 8, 413–432 (2003).
Wrangham, R. W. Two types of aggression in human evolution. Proc. Natl Acad. Sci. USA 115, 245–253 (2018).
Insel, T.R., Winslow, J.T., Wang, Z. & Young, L.J. in Vasopressin and Oxytocin (eds Zingg, H. H., Bourque, C. W. & Bichet, D.G.) 215–224 (Springer, 1998).
Goodson, J. L. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 34, 67–77 (1998).
O’Connell, L. A. & Hofmann, H. A. Evolution of a vertebrate social decision-making network. Science 336, 1154–1157 (2012).
Benarroch, E. E. Periaqueductal gray: an interface for behavioral control. Neurology 78, 210–217 (2012).
Ferris, C. F. et al. Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J. Neurosci. 17, 4331–4340 (1997).
Ferris, C. F. & Potegal, M. Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol. Behav. 44, 235–239 (1988).
Gross, C. T. & Canteras, N. S. The many paths to fear. Nat. Rev. Neurosci. 13, 651–658 (2012).
Wang, L., Chen, I. Z. & Lin, D. Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85, 1344–1358 (2015).
Lindenfors, P. & Tullberg, B. S. Evolutionary aspects of aggression the importance of sexual selection. Adv. Genet. 75, 7–22 (2011).
Eisen, E. J. & Legates, J. E. Genotype-sex interaction and the genetic correlation between the sexes for body weight in Mus musculus. Genetics 54, 611–623 (1966).
Eisenberg, J. F. Studies on the behavior of Peromyscus maniculatus gambelii and Peromyscus californicus parasiticus. Behaviour 19, 177–207 (1962).
Archer, J. Does sexual selection explain human sex differences in aggression? Behav. Brain Sci. 32, 249–266 (2009). discussion 266–311.
Harrendorf, S., Heiskanen, M. & Malby, S., eds. International Statistics on Crime and Justice. HEUNI Publication Series No. 64 (United Nations Office on Drugs and Crime, 2010).
Österman, K. et al. Cross‐cultural evidence of female indirect aggression. Aggressive Behav. 24, 1–8 (1998).
Fedy, B. C. & Stutchbury, B. J. Territory defence in tropical birds: are females as aggressive as males? Behav. Ecol. Sociobiol. 58, 414–422 (2005).
Acknowledgements
The authors thank V. Diaz for editing the manuscript. The authors also thank M. Long and E. Jarvis for their helpful comments regarding songbird brain anatomy. The authors apologize to all authors whose primary research papers could not be cited due to the limit on reference number. This work was supported by a Leon Levy Fellowship (J.E.L); the Irma T. Hirschl Trust (D.L.); and NIMH R01MH101377, R21MH105774 and 1U19NS107616-01 (to D.L.).
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Lischinsky, J.E., Lin, D. Neural mechanisms of aggression across species. Nat Neurosci 23, 1317–1328 (2020). https://doi.org/10.1038/s41593-020-00715-2
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DOI: https://doi.org/10.1038/s41593-020-00715-2
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