Sex Differences in Social Cognition.
Aggression
Androgens
Estrogens
Social Learning
Social Recognition
Journal
Current topics in behavioral neurosciences
ISSN: 1866-3370
Titre abrégé: Curr Top Behav Neurosci
Pays: Germany
ID NLM: 101535383
Informations de publication
Date de publication:
2023
2023
Historique:
pubmed:
24
5
2022
medline:
3
3
2023
entrez:
23
5
2022
Statut:
ppublish
Résumé
In this review we explore the sex differences underlying various types of social cognition. Particular focus will be placed on the behaviors of social recognition, social learning, and aggression. Known similarities and differences between sexes in the expressions of these behaviors and the known brain regions where these behaviors are mediated are discussed. The role that the sex hormones (estrogens and androgens) have as well as possible interactions with other neurochemicals, such as oxytocin, vasopressin, and serotonin is reviewed as well. Finally, implications about these findings on the mediation of social cognition are mediated and the sex differences related to humans are considered.
Identifiants
pubmed: 35604571
doi: 10.1007/7854_2022_325
doi:
Substances chimiques
Vasopressins
11000-17-2
Oxytocin
50-56-6
Types de publication
Review
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
207-234Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Agrell J, Wolff J, Ylönen H, Ylonen H (1998) Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83:507–517
Albers H (2012) The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network. Horm Behav 61(3):283–292
pubmed: 22079778
Alexander G, Hines M (2002) Sex differences in response to children’s toys in nonhuman primates (Cercopithecus aethiops sabaeus). Evol Hum Behav 23(6):467–479
Al-Maliki S, Brain P, Childs G, Benton D (1980) Factors influencing maternal attack on conspecific intruders by lactating female “TO” strain mice. Aggress Behav 6(2):103–117
Aspesi D, Choleris E (2021) Neuroendocrine underpinning of social recognition in males and females. J Neuroendocrinol. https://doi.org/10.1111/jne.13070
Aspesi D, Brill Z, Guillaume G, Choleris E (2021) Androgens and estrogens in the bed nucleus of the stria terminalis of male mice rapidly modulate social recognition and aggression, possibly interacting with vasopressin. Soc Neurosci Online P684:5
Bailey DJ, Saldanha CJ (2015) The importance of neural aromatization in the acquisition, recall, and integration of song and spatial memories in passerines. Horm Behav 74:116–124
pubmed: 26122300
pmcid: 9366902
Bakker J, Baum M (2008) Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 29(1):1–16
pubmed: 17720235
Bao A, Swaab D (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16(5):550–565
pubmed: 20889965
Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20(3):143–149
pubmed: 16701358
Bielsky I, Hu S, Szegda K, Westphal H, Young L (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29:483–493
pubmed: 14647484
Blanchard D, Blanchard R (2003) What can animal aggression research tell us about human aggression? Horm Behav 44(3):171–177
pubmed: 14609539
Blanchard D, Fukunaga-Stinson C, Takahashi L, Flannelly K, Blanchard R (1984) Dominance and aggression in social groups of male and female rats. Behav Process 9(1):31–48
Bluthe R, Dantzer R (1990) Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res 535:301–304
pubmed: 1963571
Bono A, Whiten A, van Schaik C, Krutzen M, Eichenberger F, Schnider A, van de Waal E (2018) Payoff- and sex-biased social learning interact in a wild primate population. Curr Biol 28(17):2800–2805
pubmed: 30174189
Burkart J (2017) Evolution and consequences of sociality. In: Call J, Burghardt G, Pepperberg I, Snowdon C, Zentall T (eds) APA handbook of comparative psychology: basic concepts, methods, neural substrate, and behavior. American Psychological Association, Washington, pp 257–271
Cacioppo J, Hawkey L, Norman G, Berntson G (2011) Social isolation. Ann N Y Acad Sci 1231(1):17–22
pubmed: 21651565
pmcid: 3166409
Campi K, Jameson C, Trainor B (2013) Sexual dimorphism in the brain of the monogamous California mouse (Peromyscus californicus). Brain Behav Evol 81(4):236–249
pubmed: 23881046
Catalano L, Heerey E, Gold J (2018) The valuation of social rewards in schizophrenia. J Abnorm Psychol 127(6):602–611
pubmed: 30102066
pmcid: 6101974
Chen P, Hong W (2018) Neural circuit mechanisms of social behavior. Neuron 98:16–30
pubmed: 29621486
pmcid: 6028944
Choleris E, Kavaliers M (1999) Social learning in animals: sex differences and neurobiological analysis. Pharmacol Biochem Behav 64(4):767–776
pubmed: 10593200
Choleris E, Gustafsson J, Korach K, Muglia L, Pfaff D, Ogawa S (2003) An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-α and -β knockout mice. Proc Natl Acad Sci U S A 100(10):6192–6197
pubmed: 12730370
pmcid: 156348
Choleris E, Ogawa S, Kavaliers M, Gustafsson J, Korach K, Muglia L, Pfaff D (2006) Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice. Genes Brain Behav 5(7):528–539
pubmed: 17010099
Choleris E, Little S, Mong J, Puram S, Langer R, Pfaff D (2007) Microparticle-based delivery of oxytocin receptor antisense DNA in the medial amygdala blocks social recognition in female mice. Proc Natl Acad Sci U S A 104(11):4670–4675
pubmed: 17360582
pmcid: 1838659
Choleris E, Clipperton-Allen A, Phan A, Kavaliers M (2009) Neuroendocrinology of social information processing in rats and mice. Front Neuroendocrinol 30:442–459
pubmed: 19442683
Choleris E, Clipperton-Allen A, Gray D, Diaz-Gonzalez S, Welsman R (2011) Differential effects of dopamine receptor D1-type and D2-type antagonists and phase of the estrous cycle on social learning of food preferences, feeding, and social interactions in mice. Neuropsychopharmacology 36:1689–1702
pubmed: 21525863
pmcid: 3138658
Choleris E, Clipperton-Allen A, Phan A, Valsecchi P, Kavaliers M (2012) Estrogenic involvement in social learning, social recognition and pathogen avoidance. Front Neuroendocrinol 33:140–159
pubmed: 22369749
Choleris E, Galea L, Sohrabji F, Frick K (2018) Sex differences in the brain: implications for behavioural and biomedical research. Neurosci Biobehav Rev 85:126–145
pubmed: 29287628
pmcid: 5751942
Clipperton A, Spinato J, Chernets C, Pfaff D, Choleris E (2008) Differential effects of estrogen receptor alpha and beta specific agonists on social learning of food preferences in female mice. Neuropsychopharmacology 33:2362–2375
pubmed: 18004284
Clipperton-Allen A, Cragg C, Wood A, Pfaff D, Choleris E (2010) Agonistic behavior in males and females: effects of an estrogen receptor beta agonist in gonadectomized and gonadally intact mice. Psychoneuroendocrinology 35(7):1008–1022
pubmed: 20129736
Clipperton-Allen A, Almey A, Melichercik A, Allen C, Choleris E (2011) Effects of an estrogen receptor alpha agonist on agonistic behaviour in intact and gonadectomized male and female mice. Psychoneuroendocrinology 36(7):981–995
pubmed: 21247705
Dantzer R, Bluthe R, Koob G, Le Moal M (1987) Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology 91:363–368
pubmed: 3104959
De Vries G, Buijs R, Sluiter A (1984) Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Res 298(1):141–145
pubmed: 6722551
De Vries G, Rissman E, Simerly R, Yang L, Scordalakes E, Auger C, Swain A, Lovell-Badge R, Burgoyne P, Arnold A (2002) A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J Neurosci 22(20):9005–9014
pubmed: 12388607
pmcid: 6757680
del Abril A, Segovia S, Guillamon A (1987) The bed nucleus of the stria terminalis in the rat: regional sex differences controlled by gonadal steroids early after birth. Brain Res 429:295–300
pubmed: 3567668
Dumais K, Veenema A (2016) Vasopressin and oxytocin receptor systems in the brain: sex differences and sex specific regulation of social behavior. Front Neuroendocrinol 40:1–23
pubmed: 25951955
Engelmann M, Wotjak C, Landgraf R (1995) Social discrimination procedure: an alternative method to investigate juvenile abilities in rats. Physiol Behav 58:315–321
pubmed: 7568435
Ervin K, Lymer J, Matta R, Clipperton-Allen A, Kavaliers M, Choleris E (2015a) Estrogen involvement in social behavior in rodents: rapid and long-term actions. Horm Behav 7:53–76
Ervin K, Mulvale E, Gallagher N, Roussel V, Choleris E (2015b) Activation of the G protein-coupled estrogen receptor, but not estrogen receptor α or β, rapidly enhances social learning. Psychoneuroendocrinology 58:51–66
pubmed: 25957002
Ferguson J, Young L, Hearn E, Matzuk M, Insel T, Winslow J (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288
pubmed: 10888874
Ferguson J, Aldag J, Insel T, Young L (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21(20):8278–8285
pubmed: 11588199
pmcid: 6763861
Ferri S, Abel T, Brodkin E (2018) Sex differences in autism spectrum disorder: a review. Curr Psychiatr Rep 20(9):1–17
Ferris C (2000) Adolescent stress and neural plasticity in hamsters: a vasopressin-serotonin model of inappropriate aggressive behaviour. Exp Physiol 85(s1):85S–90S
pubmed: 10795910
Fodor A, Barsvari B, Aliczki M, Balogh Z, Zelena D, Goldberg S, Haller J (2014) The effects of vasopressin deficiency on aggression and impulsiveness in male and female rats. Psychoneuroendocrinology 47:141–150
pubmed: 25001964
Forger N, Rosen G, Waters E, Jacob D, Simerly R, de Vries G (2004) Deletion of Bax eliminates sex differences in the mouse forebrain. Proc Natl Acad Sci U S A 101:13666–13671
pubmed: 15342910
pmcid: 518810
Gabor C, Phan A, Clipperton-Allen A, Kavaliers M, Choleris E (2012) Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav Neurosci 126(1):97–109
pubmed: 22141469
Gabor C, Lymer J, Phan A, Choleris E (2015) Rapid effects of the G-protein coupled oestrogen receptor (GPER) on learning and dorsal hippocampus dendritic spines in female mice. Physiol Behav 149:53–60
pubmed: 26003497
Galderisi S, Bucci P, Ucok A, Peuskens J (2012) No gender differences in social outcome in patients suffering from schizophrenia. Eur Psychiatry 27(6):406–408
pubmed: 21616645
Gogos A, Ney L, Seymour N, Rheenen T, Felmingham K (2019) Sex differences in schizophrenia, bipolar disorder, and post-traumatic stress disorder: are gonadal hormones the link? Br J Pharmacol 176(21):4119–4135
pubmed: 30658014
pmcid: 6877792
Gorski R, Gordon J, Shryne J, Southam A (1978) Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 148:333–346
pubmed: 656937
Grant E, Mackintosh J (1963) A comparison of the social postures of some common laboratory rodents. Behaviour 21(3-4):246–259
Grieb Z, Ross A, McCann K, Lee S, Welch M, Gomez M, Norvelle A, Michopoulos V, Huhman K, Albers H (2021) Sex-dependent effects of social status on the regulation of arginine-vasopressin (AVP) V1a, oxytocin (OT), and serotonin (5-HT) 1A receptor binding and aggression in Syrian hamsters (Mesocricetus auratus). Horm Behav 127:104878–104878
pubmed: 33148500
Grino P, Griffin J, Wilson J (1990) Testosterone at high concentrations interacts with the human androgen receptor similarly to dihydrotestosterone. Endocrinology 126:1165–1172
pubmed: 2298157
Gutknecht L, Waider J, Kraft S, Kriegebaum C, Holtmann B, Reif A, Schmitt A, Lesch K (2008) Deficiency of brain 5-HT synthesis but serotonergic neuron formation in Tph2 knockout mice. J Neural Transm 115(8):1127–1132
pubmed: 18665319
Gutzler S, Karom M, Erwin W, Albers H (2010) Arginine-vasopressin and the regulation of aggression in female Syrian hamsters (Mesocricetus auratus). Eur J Neurosci 31(9):1655–1663
pubmed: 20525078
Hafner H (2003) Gender differences in schizophrenia. Psychoneuroendocrinology 28(Suppl 2):17–54
pubmed: 12650680
Hay D (2007) The gradual emergence of sex differences in aggression: alternative hypotheses. Psychol Med 37(11):1527–1537
pubmed: 17335642
Hazell G, Yao S, Roper J, Prossnitz E, O’Carroll A, Lolait S (2009) Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J Endocrinol 202:223–236
pubmed: 19420011
pmcid: 2710976
Hermann H (2017) Chapter 1 – defining dominance and aggression. In: Herman H (ed) Dominance and aggression in humans and other animals: the great game of life. Academic Press
Heyes C (1994) Social learning in animals: categories and mechanism. Biol Rev 69:207–231
pubmed: 8054445
Hisasue S, Seney M, Immerman E, Forger N (2010) Control of cell number in the bed nucleus of the stria terminalis of mice: role of testosterone metabolites and estrogen receptor subtypes. J Sex Med 7:1401–1409
pubmed: 20102443
Huhman K, Solomon M, Janicki M, Harmon A, Lin S, Israel J, Jasnow A (2003) Conditioned defeat in male and female Syrian hamsters. Horm Behav 44(3):293–299
pubmed: 14609551
Imwalle D, Scordalakales E, Rissman E (2002) Estrogen receptor α influences socially motivated behaviors. Horm Behav 42:484–491
pubmed: 12488114
Ito S, Murakami S, Yamanouchi K, Arai Y (1986) Perinatal androgen exposure decreases the size of the sexually dimorphic medial preoptic nucleus in the rat. Proc Jpn Acad Ser B 62(10):408–411
Kanaya M, Tsuda M, Sagoshi S, Nagata K, Morimoto C, Thu C, Toda K, Kato S, Ogawa S, Tsukahara S (2014) Regional difference in sex steroid action on formation of morphological sex differences in the anteroventral periventricular nucleus and principal nucleus of the bed nucleus of the stria terminalis. PLoS One 9:e112616
pubmed: 25398007
pmcid: 4232352
Karlsson S, Haziri K, Hansson E, Kettunen P, Westburg L (2015) Effects of sex and gonadectomy on social investigation and social recognition in mice. BMC Neurosci 16(83):1–10
Karlsson S, Studer E, Kettunen P, Westberg L (2016) Neural androgen receptors modulate gene expression and social recognition but not social investigation. Front Behav Neurosci 10(41):1–13
Kästner N, Richter S, Urbanik S, Kunert J, Waider J, Lesch K, Kaiser S, Sachser N (2019) Brain serotonin deficiency affects female aggression. Sci Rep 9(1366):1–9
Koolhaas J, Coppens C, de Boer S, Buwalda B, Meerlo P, Timmermans P (2013) The resident-intruder paradigm: a standardized test for aggression, violence and social stress. J Vis Exp 77(4367):1–7
Korte S, Meijer O, De Kloet E, Buwalda B, Keijser J, Sluyter F, Van Oortmerssen G, Bohus B (1996) Enhanced 5-HT(1A) receptor expression in forebrain regions of aggressive house mice. Brain Res 736(1–2):338–343
pubmed: 8930340
Latham N, Mason G (2004) From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl Anim Behav Sci 86(3–4):261–289
Lonsdorf E (2016) Sex differences in nonhuman primate behavioral development. J Neurosci Res 95(1–2):213–221
Lonstein J, Gammie S (2002) Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev 26(8):869–888
pubmed: 12667494
Lukas M, Toth I, Veenema A, Neumann I (2013) Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 38:916–926
pubmed: 23102690
Lukas-Herald A, Alves-Lopes R, Montezano A, Ahmed S, Youyz R (2017) Genomic and non-genomic effects of androgens in the cardiovascular system: clinical implications. Clin Sci 131(13):1405–1418
Lymer J, Robinson A, Winters B, Choleris E (2017) Rapid effects of dorsal hippocampal G-protein coupled estrogen receptor on learning in female mice. Psychoneuroendocrinology 77:131–140
pubmed: 28033587
Lymer J, Sheppard PAS, Kuun T, Blackman A, Jani N, Mahbub S, Choleris E (2018) Estrogens and their receptors in the medial amygdala rapidly facilitate social recognition in female mice. Psychoneuroendocrinology 89:30–38
pubmed: 29309995
MacDougall-Shackleton S, Ball G (1999) Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci 22(10):432–436
pubmed: 10481186
Matsuda K, Mori H, Nugent B, Pfaff D, McCarthy M, Kawata M (2011) Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology 152(7):2760–2767
pubmed: 21586557
pmcid: 3115610
Mazzucco C, Walker H, Pawluski J, Lieblich S, Galea L (2008) ERalpha, but not ERbeta, mediates the expression of sexual behavior in the female rat. Behav Brain Res 191(1):111–117
pubmed: 18433893
McCarthy M, Nugent B, Lenz K (2018) Neuroimmunology and neuroepigenetics in the establishment of sex differences in the brain. Nat Rev Neurosci 18(8):471–484
McPhie-Lalmansingh A, Tejada L, Weaver J, Rissman E (2008) Sex chromosome complement affects social interactions in mice. Horm Behav 54(4):565–570
pubmed: 18590732
pmcid: 2561329
Miczek K, Maxson S, Fish E, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125(1-2):167–181
pubmed: 11682108
Miczek K, De Almeida R, Kravitz E, Rissman E, De Boer S, Raine A (2007) Neurobiology of escalated aggression and violence. J Neurosci 27(44):11803–11806
pubmed: 17978016
pmcid: 2667097
Morè L (2008) Intra-female aggression in the mouse (Mus musculus domesticus) is linked to the estrous cycle regularity but not to ovulation. Aggress Behav 34(1):46–50
pubmed: 17647257
Morrison T, Melloni R (2014) The role of serotonin, vasopressin, and serotonin/vasopressin interactions in aggressive behavior. Curr Top Behav Neurosci 17:189–228
pubmed: 24496652
Murray E, Hien A, de Vries G, Forger N (2009) Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology 150(9):4241–4247
pubmed: 19497973
pmcid: 2736071
Nelson R, Trainor B (2007) Neural mechanisms of aggression. Nat Rev Neurosci 8:536–546
pubmed: 17585306
Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson J (2001) Mechanisms of estrogen action. Physiol Rev 81:1535–1565
pubmed: 11581496
Nomura M, Durbak L, Chan J, Smithies O, Gustafsson J, Korach K, Pfaff D, Ogawa S (2002) Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor β knockout (βERKO) male mice. Horm Behav 41(3):288–296
pubmed: 11971662
Nomura M, Andersson S, Korach K, Gustafsson J, Pfaff D, Ogawa S (2006) Estrogen receptor-β gene disruption potentiates estrogen-inducible aggression but not sexual behaviour in male mice. Eur J Neurosci 23(7):1860–1868
pubmed: 16623843
Ogawa S, Lubahn D, Korach K, Pfaff D (1997) Behavioral effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci U S A 94(4):1476–1481
pubmed: 9037078
pmcid: 19816
Ogawa S, Washburn T, Taylor J, Lubahn D, Korach K, Pfaff D (1998) Modifications of testosterone-dependent behaviors by estrogen receptor-alpha gene disruption in male mice. Endocrinology 139(12):5058–5069
pubmed: 9832445
Ogawa S, Choleris E, Pfaff D (2004) Genetic influences on aggressive behaviors and arousability in animals. Ann N Y Acad Sci 1036:257–266
pubmed: 15817742
Ogawa S, Tsukahara S, Choleris E, Vasudevan N (2020) Estrogenic regulation of social behavior and sexually dimorphic brain formation. Neurosci Behav Rev 110:46–59
Olivier B (2005) Serotonergic mechanisms in aggression. Novartis Found Symp 268:171–183
pubmed: 16206880
Palanza P, Rodgers R, Ferrari P, Parmigiani S (1996) Effects of chlordiazepoxide on maternal aggression in mice depend on experience of resident and sex of intruder. Pharmacol Biochem Behav 54(1):175–182
pubmed: 8728555
Palanza P, Della Seta D, Ferrari P, Parmigiani S (2005) Female competition in wild house mice depends upon timing of female/male settlement and kinship between females. Anim Behav 69(6):1259–1271
Paletta P, Sheppard P, Matta R, Ervin K, Choleris E (2018) Rapid effects of estrogens on short-term memory: possible mechanism. Horm Behav 104:88–99
pubmed: 29847771
Patchev A, Gotz F, Rohde W (2004) Differential role of estrogen receptor isoforms in sex-specific brain organization. FASEB J 18:1568–1570
pubmed: 15289439
Paul L, Gronek J, Politch J (1980) Maternal aggression in mice: protection of young is a by-product of attacks at the home site. Aggress Behav 6(1):19–29
Peeters D, de Boer S, Terneusen A, Newman-Tancredi A, Varney M, Verkes R, Homberg J (2019) Enhanced aggressive phenotype of Tph2 knockout rats is associated with diminished 5-HT1A receptor sensitivity. Neuropharmacology 153:134–141
pubmed: 31078489
Phan A, Lancaster K, Armstrong J, MacLusky N, Choleris E (2011) Rapid effects of estrogen receptor α and β selective agonists on learning and dendritic spines in female mice. Neuroendocrinology 152(4):1492–1502
Phan A, Gabor S, Favaro K, Kaschack S, Armstrong J, MacLusky N, Choleris E (2012) Low doses of 17β-estradiol rapidly improve learning and increase hippocampal dendritic spines. Neuropsychopharmacology 37:2299–2309
pubmed: 22669167
pmcid: 3422494
Phan A, Suschkov S, Molinaro L, Reynolds K, Lymer J, Bailey C, Kow L, MacLusky N, Pfaff D, Choleris E (2015) Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements. Proc Natl Acad Sci U S A 112(52):16018–16023
pubmed: 26655342
pmcid: 4703013
Pierman S, Sica M, Allieri F, Viglietti-Panzica C, Panzica G, Bakker J (2008) Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene. Horm Behav 54:98–106
pubmed: 18346740
pmcid: 2706693
Potegal M, Ferris C (1989) Intraspecific aggression in male hamsters is inhibited by intrahypothalamic vasopressin-receptor antagonist. Aggress Behav 15(4):311–320
Raynaud JP (1973) Influence of rat estradiol binding plasma protein (EBP) on uterotrophic activity. Steroids 21(2):249–258
pubmed: 4689748
Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11(11):1327–1334
pubmed: 18820691
pmcid: 2577388
Rosell D, Siever L (2015) The neurobiology of aggression and violence. CNS Spectr 20(3):254–279
pubmed: 25936249
Rosvall K (2011) Intrasexual competition in females: evidence for sexual selection? Behav Ecol 22(6):1131–1140
pubmed: 22479137
pmcid: 3199163
Rowell T (1970) Baboon menstrual cycles affected by social environment. J Reprod Fertil 21:133–141
pubmed: 4983966
Sanchez-Andrade G, Kendrick K (2011) Roles of α- and β-estrogen receptors in mouse social recognition memory: effects of gender and the estrous cycle. Horm Behav 59:114–122
pubmed: 21056567
Sawyer T, Hengehold A, Perez W (1984) Chemosensory and hormonal mediation of social memory in male rats. Behav Neurosci 98:908–913
pubmed: 6487419
Schulz K, Zehr J, Salas-Ramirez K, Sisk C (2009) Testosterone programs adult social behavior before and during, but not after, adolescence. Endocrinology 150:3690–3698
pubmed: 19423759
pmcid: 2717880
Sheppard P, Koss W, Frick K, Choleris E (2018) Rapid actions of oestrogens and their receptors on memory acquisition and consolidation in females. J Neuroendocrinol 30(2):1–10
Silk J (2007) The adaptive value of sociality in mammalian groups. Philos Trans R Soc Lond B Biol Sci 362:539–559
pubmed: 17363359
pmcid: 2346516
Smith C, DiBenedictis B, Veenema A (2019) Comparing vasopressin and oxytocin fiber and receptor density patterns in the social behaviour neural network: implications for cross-system signaling. Front Neuroendocrinol 53:1–16
Soma K, Scotti M, Newman A, Charlier T, Demas G (2008) Novel mechanisms for neuroendocrine regulation of aggression. Front Neuroendocrinol 29(4):476–489
pubmed: 18280561
Song Z, Albers H (2018) Cross-talk among oxytocin and arginine-vasopressin receptors: relevance for basic and clinical studies of the brain and periphery. Front Neuroendocrinol 51:14–24
pubmed: 29054552
Spiteri T, Agmo A (2009) Ovarian hormones modulate social recognition in female rats. Physiol Behav 98(1-2):247–250
pubmed: 19447123
Stoop R (2012) Neuromodulation by oxytocin and vasopressin. Neuron 76(1):142–159
pubmed: 23040812
Stribley J, Carter C (1999) Developmental exposure to vasopressin increases aggression in adult prairie voles. Proc Natl Acad Sci U S A 96(22):12601–12604
pubmed: 10535968
pmcid: 23008
Suzuki S, Handa R (2005) Estrogen receptor-beta, but not estrogen receptor-alpha, is expressed in prolactin neurons of the female rat paraventricular and supraoptic nuclei: comparison with other neuropeptides. J Comp Neurol 484:28–42
pubmed: 15717309
Takayanagi Y, Yoshida M, Bielsky I, Ross H, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk M, Young L, Nishimori K (2005) Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 102(44):16096–16101
pubmed: 16249339
pmcid: 1276060
Tan O, Musullulu H, Raymond J, Wilson B, Langguth M, Bowen M (2019) Oxytocin and vasopressin inhibit hyper-aggressive behaviour in socially isolated mice. Neuropharmacology 156:107573
pubmed: 30885607
Tang A, Nakazawa M, Romeo R, Reeb B, Sisti H, McEwen B (2005) Effects of long-term estrogen replacement on social investigation and social memory in ovariectomized C57BL/6 mice. Horm Behav 47:350–357
pubmed: 15708765
Terranova J, Song Z, Larkin T, Hardcastle N, Norvelle A, Riaz A, Albers H (2016) Serotonin and arginine-vasopressin mediate sex differences in the regulation of dominance and aggression by the social brain. Proc Natl Acad Sci U S A 113(46):13233–13238
pubmed: 27807133
pmcid: 5135349
Tsukahara S, Tsuda M, Kurihara R, Kato Y, Kuroda Y, Nakata M, Xiao K, Nagata K, Toda K, Ogawa S (2011) Effects of aromatase or estrogen receptor gene deletion on masculinization of the principal nucleus of the bed nucleus of the stria terminalis of mice. Neuroendocrinology 94:137–147
pubmed: 21525731
Unger E, Burke K, Yang C, Bender K, Fuller P, Shah N (2015) Medial amygdalar aromatase neurons regulate aggression in both sexes. Cell Rep 10(4):453–462
pubmed: 25620703
pmcid: 4349580
Vaillancourt T (2013) Do human females use indirect aggression as an intrasexual competition strategy? Philos Trans R Soc Lond B Biol Sci 368(1631):20130080
pubmed: 24167310
pmcid: 3826209
Van de Waal E, Renevey N, Favre CM, Bshary R (2010) Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc R Soc B Biol Sci 277(1691):2105–2111
Veenema A, Bredewold R, De Vries G (2012) Vasopressin regulates social recognition in juvenile and adult rats of both sexes, but in sex- and age-specific ways. Horm Behav 61:50–56
pubmed: 22033278
Vivanti G, Nuske H (2017) Autism, attachment, and social learning: three challenges and a way forward. Behav Brain Res 325:251–259
pubmed: 27751811
Wang T, Han W, Wang B, Jiang Q, Solberg-Woods L, Palmer A, Chen H (2014) Propensity for social interaction predicts nicotine-reinforced behaviors in outbred rats. Genes Brain Behav 13:202–212
pubmed: 24289793
Wersinger S, Ginns E, O'Carrol A, Lolait S, Young W (2002) Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol Psychiatry 7:975–984
pubmed: 12399951
Wharton A (2009) The sociology of gender: an introduction to theory and research. Wiley
Whiten A, van de Waal E (2018) The pervasive role of social learning in primate lifetime development. Behav Ecol Sociobiol 72:80
pubmed: 29755181
pmcid: 5934467
Whylings J, Rigney N, Peters N, De Vries G, Petrulis A (2020) Sexually dimorphic role of BNST vasopressin cells in sickness and social behavior in male and female mice. Brain Behav Immun 83:68–77
pubmed: 31550501
Wranghama R (2017) Two types of aggression in human evolution. Proc Natl Acad Sci U S A 115(2):245–253
Wu M, Manoli D, Fraser E, Coats J, Tollkuhn J, Honda S, Harada N, Shah N (2009) Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139(1):61–72
pubmed: 19804754
pmcid: 2851224