Aggression · Social interactions · Social experience · Mating · Winner effect · Neuronal plasticity · Social isolation · Oxytocin · Vasopressin · Sex hormones · Estrogen receptor α · Lateral septum · Nucleus accumbens · Ventromedial hypothalamus
Abstract :
[en] Rodent models have been extensively used to study the neural underpinnings of
aggression. Yet, the role of some external factors such as social experiences, or
internal factors such as biological sex, have only recently gained attention. This
chapter discusses how the composition of the social environment and/or the lack
of social contact (social isolation) in different stages of development impact the
display of aggressive behavior in rodents. Additionally, this chapter covers how
biological sex interacts with changes in the composition of the social environment
to affect the neuronal networks of aggression. From a neurobiological point of
view, this chapter focuses particularly on the participation of neuroendocrine
systems such as sex hormones, oxytocin, and vasopressin and on how social
interactions shape brain plasticity within those systems.
Disciplines :
Neurosciences & behavior
Author, co-author :
De Moura Oliveira, Vinicius Elias ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Animal Models of Aggression: the Role of Sex and Social Experience
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Bibliography
Aleyasin XH, Flanigan XME, Golden XSA, Takahashi XA, Menard XC, Pfau ML, Multer J, Pina XJ, Mccabe XKA, Bhatti N, Hodes GE, Heshmati M, Neve RL, Nestler XEJ, Heller XEA, Russo XSJ (2018) Cell-type-specific role of? FosB in nucleus accumbens in modulating intermale aggression. J Neurosci 38(26):5913–5924. https://doi.org/10.1523/JNEUROSCI.0296-18.2018
Allaman-Exertier G, Reymond-Marron I, Tribollet E, Raggenbass M (2007) Vasopressin modulates lateral septal network activity via two distinct electrophysiological mechanisms. Eur J Neurosci 26(September):2633–2642. https://doi.org/10.1111/j.1460-9568.2007.05866.x
Aubry A, Burnett CJ, Goodwin NL, Li L, Navarrete J, Zhang Y, Tsai V, Durand-De Cuttoli R, Golden SA, Russo SJ (2022a) Dynamic sex differences in appetitive and reactive aggression. BioRxiv. https://doi.org/10.1101/2022.02.22.481480
Aubry AV, Joseph Burnett C, Goodwin NL, Li L, Navarrete J, Zhang Y, Tsai V, Durand de Cuttoli R, Golden SA, Russo SJ (2022b) Sex differences in appetitive and reactive aggression. Neuropsychopharmacology 47:1746. https://doi.org/10.1038/s41386-022-01375-5
Bayless DW, Yang T, Mason MM, Susanto AAT, Lobdell A, Shah NM (2019) Limbic neurons shape sex recognition and social behavior in sexually naive males. Cell 176(5):1190–1205.e20. https://doi.org/10.1016/j.cell.2018.12.041
Been LE, Moore KM, Kennedy BC, Meisel RL (2016) Metabotropic glutamate receptor and fragile x signaling in a female model of escalated aggression. Biol Psychiatry 79(8):685–692. https://doi.org/10.1016/j.biopsych.2015.07.021
Been LE, Gibbons AB, Meisel RL (2019) Towards a neurobiology of female aggression. Neuropsychopharmacology 156(107451). https://doi.org/10.1016/j.neuropharm.2018.11.039.Towards
Beiderbeck DI, Reber SO, Havasi A, Bredewold R, Veenema AH, Neumann ID (2012) High and abnormal forms of aggression in rats with extremes in trait anxiety – involvement of the dopamine system in the nucleus accumbens. Psychoneuroendocrinology 37(12):1969–1980
Biro L, Toth M, Sipos E, Bruzsik B, Tulogdi A, Bendahan S, Sandi C, Haller J (2016) Structural and functional alterations in the prefrontal cortex after post-weaning social isolation: relationship with species-typical and deviant aggression. Brain Struct Funct 4(September):1–15. https://doi.org/10.1007/s00429-016-1312-z
Biro L, Sipos E, Bruzsik B, Farkas I, Zelena D, Balazsfi D, Toth M, Haller J (2018) Task division within the prefrontal cortex: distinct neuron populations selectively control different aspects of aggressive behavior via the hypothalamus. J Neurosci 38(17):4065–4075. https://doi.org/10.1523/JNEUROSCI.3234-17.2018
Borland JM, Walton JC, Norvelle A, Grantham KN, Aiani LM, Larkin TE, McCann KE, Albers HE (2019) Social experience and sex-dependent regulation of aggression in the lateral septum by extrasynaptic dGABAA receptors. Psychopharmacology 237(2):329–344. https://doi.org/10.1007/s00213-019-05368-z
Bosch OJ (2013) Maternal aggression in rodents: brain oxytocin and vasopressin mediate pup defence. Philos Trans R Soc B: Biol Sci 368(1631):20130085. https://doi.org/10.1098/rstb.2013.0085
Bosch OJ, Krömer SA, Brunton PJ, Neumann ID (2004) Release of oxytocin in the hypothalamic paraventricular nucleus, but not central amygdala or lateral septum in lactating residents and virgin intruders during maternal defence. Neuroscience 124(2):439–448. https://doi.org/10.1016/j.neuroscience.2003.11.028
Bosch OJ, Meddle SL, Beiderbeck DI, Douglas AJ, Neumann ID (2005) Brain oxytocin correlates with maternal aggression: link to anxiety. J Neurosci 25(29):6807–6815. https://doi.org/10.1523/JNEUROSCI.1342-05.2005
Bowler CM, Cushing BS, Carter CS (2002) Social factors regulate female-female aggression and affiliation in prairie voles. Physiol Behav 76:559–566
Calcagnoli F, De Boer SF, Althaus M, Den Boer JA, Koolhaas JM (2013) Antiaggressive activity of central oxytocin in male rats. Psychopharmacology 229(4):639–651. https://doi.org/10.1007/s00213-013-3124-7
Calcagnoli F, Kreutzmann JC, de Boer SF, Althaus M, Koolhaas JM (2015) Acute and repeated intranasal oxytocin administration exerts anti-aggressive and pro-affiliative effects in male rats. Psychoneuroendocrinology 51:112–121. https://doi.org/10.1016/j.psyneuen.2014.09.019
Campbell A (1999) Staying alive: evolution, culture, and women’s intrasexual aggression. Behav Brain Sci 22(2):203–252. https://doi.org/10.1017/S0140525X99001818
Chase ID, Bartolomeo C, Dugatkin LA et al (1994) Aggressive interactions and inter-contest interval: how long winner keep winning? Anim Behav 48(July):393400
Dai B, Sun F, Tong X, Ding Y, Kuang A, Osakada T, Li Y, Lin D (2022) Responses and functions of dopamine in nucleus accumbens core during social behaviors. Cell Rep 40(8):111246. https://doi.org/10.1016/j.celrep.2022.111246
De Almeida RMM, Ferrari PF, Parmigiani S, Miczek KA (2005) Escalated aggressive behavior: dopamine, serotonin and GABA. Eur J Pharmacol 526(1–3):51–64. https://doi.org/10.1016/j.ejphar.2005.10.004
de Figueiredo CS, Sandre PC, Portugal LCL, Mázala-de-Oliveira T, da Silva Chagas L, Raony Í, Ferreira ES, Giestal-de-Araujo E, dos Santos AA, Bomfim POS (2021) COVID-19 pandemic impact on children and adolescents’ mental health: biological, environmental, and social factors. Prog Neuro-Psychopharmacol Biol Psychiatry 106:110171. https://doi.org/10.1016/j.pnpbp.2020.110171
de Jong TR, Neumann ID (2017) Oxytocin and aggression. Curr Topics Behav Neurosci 35(September):1–18
Elliott Albers H, Dean A, Karom MC, Smith D, Huhman KL (2006) Role of V1a vasopressin receptors in the control of aggression in Syrian hamsters. Brain Res 1073–1074(1):425–430. https://doi.org/10.1016/j.brainres.2005.12.081
Falkner AL, Grosenick L, Davidson TJ, Deisseroth K, Lin D (2016) Hypothalamic control of male aggression-seeking behavior. Nat Neurosci 19(4):596–604. https://doi.org/10.1038/nn.4264
Golden SA, Heins C, Venniro M, Caprioli D, Zhang M, Epstein DH, Shaham Y (2017) Compulsive addiction-like aggressive behavior in mice. Biol Psychiatry 82(4):239–248. https://doi.org/10.1016/j.biopsych.2017.03.004
Golden SA, Jin M, Heins C, Venniro M, Michaelides M, Shaham Y (2019) Nucleus accumbens Drd1-expressing neurons control aggression self-administration and aggression seeking in mice. J Neurosci 18(2):2409. https://doi.org/10.1523/JNEUROSCI.2409-18.2019
Gubernick DJ, Alberts JR (1987) The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol 101(2):169
Haller J (2013) The neurobiology of abnormal manifestations of aggression-a review of hypothalamic mechanisms in cats, rodents, and humans. Brain Res Bull 93(2010):97–109. https://doi.org/10.1016/j.brainresbull.2012.10.003
Hashikawa K, Hashikawa Y, Tremblay R, Zhang J, Feng JE, Sabol A, Piper WT, Lee H, Rudy B, Lin D (2017) Esr1+cells in the ventromedial hypothalamus control female aggression. Nat Neurosci 20(11):1580–1590. https://doi.org/10.1038/nn.4644
Hashikawa K, Hashikawa Y, Lischinsky J, Lin D (2018) The neural mechanisms of sexually dimorphic aggressive behaviors. Trends Genet 10(October):755–776. https://doi.org/10.1016/j.tig.2018.07.001
Ho HP, Olsson M, Westberg L, Melke J, Eriksson E (2001) The serotonin reuptake inhibitor fluoxetine reduces sex steroid-related aggression in female rats: an animal model of premenstrual irritability? Neuropsychopharmacology 24(5):502–510. https://doi.org/10.1016/S0893-133X(00)00219-0
Hsu Y, Earley RL, Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev Camb Philos Soc 81(1):33–74. https://doi.org/10.1017/S146479310500686X
Karelina K, Walton JC, Weil ZM, Norman GJ, Nelson RJ, DeVries AC (2010) Estrous phase alters social behavior in a polygynous but not a monogamous Peromyscus species. Horm Behav 58(2):193–199. https://doi.org/10.1016/j.yhbeh.2010.03.022
Kim HHS, Jung JH (2021) Social isolation and psychological distress during the COVID-19 pandemic: a cross-national analysis. Gerontologist 61(1):103–113. https://doi.org/10.1093/geront/gnaa168
Koolhaas JM, Schuurman T, Wiepkema PR (1980) The organization of intraspecific agonistic behaviour in the rat. Prog Neurobiol 15(3):247–268. https://doi.org/10.1016/0301-0082(80)90024-6
Koolhaas JM, Coppens CM, de Boer SF, Buwalda B, Meerlo P, Timmermans PJ (2013) The resident-intruder paradigm: A standardized test for aggression, violence and social stress. J Vis Exp 77(77):4367
Lee H, Kim D-W, Remedios R, Anthony TE, Chang A, Madisen L, Zeng H, Anderson DJ (2014) Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus. Nature 509(7502):627–632. https://doi.org/10.1038/nature13169
Lenschow C, Lima SQ (2020) In the mood for sex: neural circuits for reproduction. Curr Opin Neurobiol 60(December):155–168. https://doi.org/10.1016/j.conb.2019.12.001
Leroy F, Park J, Asok A, Brann DH, Meira T, Boyle LM, Eric W, Siegelbaum SA (2018) A circuit from hippocampal CA2 to lateral septum disinhibits social aggression. Nature 564(7735):213–218. https://doi.org/10.1038/s41586-018-0772-0
Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470(7333):221–226. https://doi.org/10.1038/nature09736
Lischinsky JE, Lin D (2020) Neural mechanisms of aggression across species. Nat Neurosci 23(11):1317–1328. https://doi.org/10.1038/s41593-020-00715-2
Liu M, Kim D-W, Zeng H, Anderson DJ (2022) Make war not love: the neural substrate underlying a state-dependent switch in female social behavior. Neuron 110:841. https://doi.org/10.1016/j.neuron.2021.12.002
Ludwig M, Leng G (2006) Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci 7(2):126–136. https://doi.org/10.1038/nrn1845
Lukas M, de Jong TR (2017) Conspecific interactions in adult laboratory rodents: friends or foes? In: Wöhr M, Krach S (eds) Social behavior from rodents to humans: neural foundations and clinical implications, pp 3–24. https://doi.org/10.1007/7854_2015_428.Springer International Publishing
Lukas M, Suyama H, Egger V (2019) Vasopressin cells in the rodent olfactory bulb resemble non-bursting superficial tufted cells and are primarily inhibited upon olfactory nerve stimulation. ENeuro 6(4):ENEURO.0431. https://doi.org/10.1523/ENEURO.0431-18.2019
Masis-Calvo M, Schmidtner AK, de Moura Oliveira VE, Grossmann CP, de Jong TR, Neumann ID (2018) Animal models of social stress: the dark side of social interactions. Stress 5(September):41–432. https://doi.org/10.1080/10253890.2018.1462327
Menon R, Grund T, Zoicas I, Eliava M, Grinevich V, Neumann ID, Menon R, Grund T, Zoicas I, Althammer F, Fiedler D, Biermeier V, Bosch OJ, Hiraoka Y, Nishimori K, Eliava M, Grinevich V (2018) Oxytocin signaling in the lateral septum prevents social fear during lactation. Curr Biol 28(2):1–13. https://doi.org/10.1016/j.cub.2018.02.044
Menon R, Süß T, Oliveira VE d M, Neumann ID, Bludau A (2021) Neurobiology of the lateral septum: regulation of social behavior. Trends Neurosci 5:27–40. https://doi.org/10.1016/j.tins.2021.10.010
Miczek KA, Maxson SC, Fish EW, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125(1–2):167–181
Miczek KA, de Boer SF, Haller J (2013) Excessive aggression as model of violence: A critical evaluation of current preclinical methods. Psychopharmacology 226(3):445–458. https://doi.org/10.1007/s00213-013-3008-x
Mikics É, Guirado R, Umemori J, Miskolczi C, Karpova NN, Castre E, Guirado R, Umemori J (2017) Social learning requires plasticity enhanced by fluoxetine through prefrontal Bdnf-TrkB signaling to limit aggression induced by post-weaning social isolation. Neuropsychopharmacology 43:235. https://doi.org/10.1038/npp.2017.142
Mojahed A, Brym S, Hense H, Grafe B, Helfferich C, Lindert J, Garthus-Niegel S (2021) Rapid review on the associations of social and geographical isolation and intimate partner violence: implications for the ongoing COVID-19 pandemic. In: Frontiers in psychiatry, vol 12. Frontiers Media S.A. https://doi.org/10.3389/fpsyt.2021.578150
Nelson RJ, Trainor BC (2007) Neural mechanisms of aggression. Nat Rev Neurosci 8(7):536–546
Newman SW (1999) The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 877:242–257. https://doi.org/10.1111/j.1749-6632.1999.tb09271.x
Newman EL, Covington HE III, Suh J, Bicakci MB, Ressler KJ, Debold JF, Miczek KA (2019) Fighting females: neural and behavioral consequences of social defeat stress in female mice. Biol Psychiatry 86(9):657–668. https://doi.org/10.1016/j.biopsych.2019.05.005
Nordman JC, Ma X, Gu Q, Potegal M, Li H, Kravitz AV, Li Z (2020) Potentiation of divergent medial amygdala pathways drives experience-dependent aggression escalation. J Neurosci 40(25):4858–4880. https://doi.org/10.1523/JNEUROSCI.0370-20.2020
Nyuyki KD, Waldherr M, Baeuml S, Neumann ID (2011) Yes, I am ready now: differential effects of paced versus unpaced mating on anxiety and central oxytocin release in female rats. PLoS One 6(8):e23599. https://doi.org/10.1371/journal.pone.0023599
Oliveira VE d M, Bakker J (2022) Neuroendocrine regulation of female aggression. In: Frontiers in endocrinology, vol 13. Frontiers Media S.A. https://doi.org/10.3389/fendo.2022.957114
Oliveira VEM, Neumann ID, de Jong TR (2019) Post-weaning social isolation exacerbates aggression in both sexes and affects the vasopressin and oxytocin system in a sex-specific manner. Neuropharmacology156(October 2018):107504. https://doi.org/10.1016/j.neuropharm.2019.01.019
Oliveira VEM, Lukas M, Wolf HN, Durante E, Lorenz A, Mayer A-L, Bludau A, Bosch OJ, Grinevich V, Egger V, de Jong TR, Neumann ID (2021) Oxytocin and vasopressin within the ventral and dorsal lateral septum modulate aggression in female rats. Nat Commun 12(1):1–15. https://doi.org/10.1038/s41467-021-23064-5
Oliveira VEM, de Jong TR, Neumann ID (2022a) Modelling sexual violence in male rats: the sexual aggression test (SxAT). Transl Psychiatry 12(207):1–12. https://doi.org/10.1038/s41398-022-01973-3
Oliveira VEM, de Jong TR, Neumann ID (2022b) Synthetic oxytocin and vasopressin act within the central amygdala to exacerbate aggression in female Wistar rats. Front Neurosci 16(May):1–12. https://doi.org/10.3389/fnins.2022.906617
Otroen M (1990) Short communications the effect of prior experience on the outcome of fights in the burying beetle, nicrophorus humator fights. Anim Behav 40(5):980–1004
Oyegbile TO, Marler CA (2005) Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm Behav 48(3):259–267. https://doi.org/10.1016/j.yhbeh.2005.04.007
Qian T, Wang H, Wang P, Geng L, Mei L, Osakada T, Wang L, Tang Y, Kania A, Grinevich V, Stoop R, Lin D, Luo M, Li Y (2023) A genetically encoded sensor measures temporal oxytocin release from different neuronal compartments. Nat Biotechnol. https://doi.org/10.1038/s41587-022-01561-2
Raggenbass M, Tribollet E, Dreifuss JJ (1987) Electrophysiological and autoradiographical evidence of V1 vasopressin receptors in the lateral septum of the rat brain. Proc Natl Acad Sci U S A 84(21):7778–7782. https://doi.org/10.1073/pnas.84.21.7778
Reidy DE, Kearns MC, DeGue S (2013) Reducing psychopathic violence: a review of the treatment literature. Aggress Violent Behav 18(5):527–538. https://doi.org/10.1016/j.avb.2013.07.008
Reidy DE, Kearns MC, DeGue S, Lilienfeld SO, Massetti G, Kiehl KA (2015) Why psychopathy matters: implications for public health and violence prevention. Aggress Violent Behav 24:214–225. https://doi.org/10.1016/j.avb.2015.05.018
Remedios R, Kennedy A, Zelikowsky M, Grewe BF, Schnitzer MJ, Anderson DJ (2017) Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex. Nature 550(7676):388–392. https://doi.org/10.1038/nature23885
Rosenthal GG, Ryan MJ (2022) Sexual selection and the ascent of women: mate choice research since Darwin. Science 375(6578):eabi6308. https://doi.org/10.1126/science.abi6308. American Association for the Advancement of Science
Ross AP, Mccann KE, Larkin TE, Song Z, Grieb ZA, Huhman KL, Albers HE (2019) Sex-dependent effects of social isolation on the regulation of arginine-vasopressin (AVP) V1a, oxytocin (OT) and serotonin (5HT) 1a receptor binding and aggression. Horm Behav 116(June):104578. https://doi.org/10.1016/j.yhbeh.2019.104578
Ruscio MG, King SB, Kinley-Cooper SK, McKendrick G (2018) Social environment affects central distribution of estrogen receptor-a in Peromyscus californicus. Gen Comp Endocrinol 269:81–87. https://doi.org/10.1016/j.ygcen.2018.08.018
Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16(5):290–304
Sayegh JF, Kobor G, Lajtba A, Vadasz C (n.d.) Effects of social isolation and the time of day on testosterone levels in plasma of CS7BLMiBy and BALBlcBy mice
Schuett GW (1997) Body size and agonistic experience affect dominance and mating success in male copperheads. Anim Behav 54(1):213–224. https://doi.org/10.1006/anbe.1996.0417
Silva AL, Fry WHD, Sweeney C, Trainor BC (2010) Effects of photoperiod and experience on aggressive behavior in female California mice. Behav Brain Res 208(2):528–534. https://doi.org/10.1016/j.bbr.2009.12.038
Staffend NA, Meisel RL (2012) Aggressive experience increases dendritic spine density within the nucleus accumbens core in female Syrian hamsters. Neuroscience 227:163–169. https://doi.org/10.1016/j.neuroscience.2012.09.064
Stagkourakis S, Spigolon G, Liu G, Anderson DJ (2020) Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.2011782117/-/DCSupplemental
Sumner SA, Mercy JA, Dahlberg LL, Hillis SD, Klevens J, Houry D (2015) Violence in the United States: status, challenges, and opportunities. JAMA 314(5):478–488. https://doi.org/10.1001/jama.2015.8371
Suyama H, Egger V, Lukas M (2021) Top-down acetylcholine signaling via olfactory bulb vasopressin cells contributes to social discrimination in rats. Commun Biol 4(1):603. https://doi.org/10.1038/s42003-021-02129-7
Terwilliger EF, Young LJ (2014) Diversity in behaviors related to monogamy in prairie voles. 63(3):518–526. https://doi.org/10.1016/j.yhbeh.2013.01.005.Variation
Tobin VA, Hashimoto H, Wacker DW, Takayanagi Y, Langnaese K, Caquineau C, Noack J, Landgraf R, Onaka T, Leng G, Meddle SL, Engelmann M, Ludwig M (2010) An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 464(7287):413–417. https://doi.org/10.1038/nature08826
Toth M, Mikics E, Tulogdi A, Aliczki M, Haller J (2011) Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm Behav 60(1):28–36. https://doi.org/10.1016/j.yhbeh.2011.02.003
Toth M, Tulogdi A, Biro L, Soros P, Mikics E, Haller J (2012) The neural background of hyper-emotional aggression induced by post-weaning social isolation. Behav Brain Res 233(1):120–129. https://doi.org/10.1016/j.bbr.2012.04.025
Trainor BC, Workman JL, Jessen R, Nelson RJ (2007) Impaired nitric oxide synthase signaling dissociates social investigation and aggression. Behav Neurosci 121(2):362–369. https://doi.org/10.1037/0735-7044.121.2.362
Trainor BC, Takahashi EY, Silva AL, Crean KK, Hostetler C (2010) Sex differences in hormonal responses to social conflict in the monogamous California mouse. Horm Behav 58(3):506–512. https://doi.org/10.1016/j.yhbeh.2010.04.008
Tulogdi Á, Tóth M, Barsvári B, Biró L, Mikics É, Haller J (2014) Effects of resocialization on post-weaning social isolation-induced abnormal aggression and social deficits in rats. Dev Psychobiol 56(1):49–57. https://doi.org/10.1002/dev.21090
Veenema AH, Beiderbeck DI, Lukas M, Neumann ID (2010) Distinct correlations of vasopressin release within the lateral septum and the bed nucleus of the stria terminalis with the display of intermale aggression. Horm Behav 58(2):273–281. https://doi.org/10.1016/j.yhbeh.2010.03.006
Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci U S A 104(42):16681–16684. https://doi.org/10.1073/pnas.0705860104
Wei D, Talwar V, Lin D (2021) Neural circuits of social behaviors: innate yet flexible. Neuron 109(10):1600–1620. https://doi.org/10.1016/j.neuron.2021.02.012
Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, Honda SI, Harada N, Shah NM (2009) Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139(1):61–72. https://doi.org/10.1016/j.cell.2009.07.036
Yamaguchi T (2022) Neural circuit mechanisms of sex and fighting in male mice. In: Neuroscience research, vol 174. Elsevier Ireland Ltd, pp 1–8. https://doi.org/10.1016/j.neures.2021.06.005
Yang CF, Chiang MC, Gray DC, Prabhakaran M, Alvarado M, Juntti SA, Unger EK, Wells JA, Shah NM (2013) Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153(4):896–909. https://doi.org/10.1016/j.cell.2013.04.017
Yang T, Yang CF, Chizari MD, Bender KJ, Ganguli S, Shah NM (2017) Social control of hypothalamus-mediated male article social control of hypothalamus-mediated male aggression. Neuron 95(4):955–970.e4. https://doi.org/10.1016/j.neuron.2017.06.046
Yang B, Karigo T, Anderson DJ (2022a) Transformations of neural representations in a social behaviour network. Nature 608(7924):741–749. https://doi.org/10.1038/s41586-022-05057-6
Yang L, Cui J, Zeng L, Lu W (2022b) Targeting PSD95/nNOS by ZL006 alleviates social isolation-induced heightened attack behavior in mice. Psychopharmacology 239(1):267–276. https://doi.org/10.1007/s00213-021-06000-9
Yin L, Lin D (2023) Neural control of female sexual behaviors. Horm Behav 151:105339. https://doi.org/10.1016/j.yhbeh.2023.105339
Yin L, Hashikawa K, Hashikawa Y, Osakada T, Lischinsky JE, Diaz V, Lin D (2022) VMHvllCckar cells dynamically control female sexual behaviors over the reproductive cycle. Neuron 110:3000. https://doi.org/10.1016/j.neuron.2022.06.026
Zelikowsky M, Hui M, Karigo T, Choe A, Yang B, Blanco MR, Beadle K, Gradinaru V, Deverman BE, Anderson DJ (2018) The neuropeptide Tac2 controls a distributed brain state induced by chronic social isolation stress. Cell 173(5):1265–1279.e19. https://doi.org/10.1016/j.cell.2018.03.037
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