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Sex Differences in Social Cognition

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Sex Differences in Brain Function and Dysfunction

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 62))

Abstract

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.

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References

  • Agrell J, Wolff J, Ylönen H, Ylonen H (1998) Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83:507–517

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bakker J, Baum M (2008) Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 29(1):1–16

    CAS  PubMed  Google Scholar 

  • Bao A, Swaab D (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16(5):550–565

    PubMed  Google Scholar 

  • Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20(3):143–149

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Blanchard D, Blanchard R (2003) What can animal aggression research tell us about human aggression? Horm Behav 44(3):171–177

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Bluthe R, Dantzer R (1990) Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res 535:301–304

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Cacioppo J, Hawkey L, Norman G, Berntson G (2011) Social isolation. Ann N Y Acad Sci 1231(1):17–22

    PubMed  PubMed Central  Google Scholar 

  • 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  Google Scholar 

  • Catalano L, Heerey E, Gold J (2018) The valuation of social rewards in schizophrenia. J Abnorm Psychol 127(6):602–611

    PubMed  PubMed Central  Google Scholar 

  • Chen P, Hong W (2018) Neural circuit mechanisms of social behavior. Neuron 98:16–30

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choleris E, Kavaliers M (1999) Social learning in animals: sex differences and neurobiological analysis. Pharmacol Biochem Behav 64(4):767–776

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choleris E, Clipperton-Allen A, Phan A, Kavaliers M (2009) Neuroendocrinology of social information processing in rats and mice. Front Neuroendocrinol 30:442–459

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Dantzer R, Bluthe R, Koob G, Le Moal M (1987) Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology 91:363–368

    CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • 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  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Engelmann M, Wotjak C, Landgraf R (1995) Social discrimination procedure: an alternative method to investigate juvenile abilities in rats. Physiol Behav 58:315–321

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferri S, Abel T, Brodkin E (2018) Sex differences in autism spectrum disorder: a review. Curr Psychiatr Rep 20(9):1–17

    Google Scholar 

  • Ferris C (2000) Adolescent stress and neural plasticity in hamsters: a vasopressin-serotonin model of inappropriate aggressive behaviour. Exp Physiol 85(s1):85S–90S

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Grant E, Mackintosh J (1963) A comparison of the social postures of some common laboratory rodents. Behaviour 21(3-4):246–259

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Grino P, Griffin J, Wilson J (1990) Testosterone at high concentrations interacts with the human androgen receptor similarly to dihydrotestosterone. Endocrinology 126:1165–1172

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

  • Hafner H (2003) Gender differences in schizophrenia. Psychoneuroendocrinology 28(Suppl 2):17–54

    PubMed  Google Scholar 

  • Hay D (2007) The gradual emergence of sex differences in aggression: alternative hypotheses. Psychol Med 37(11):1527–1537

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Heyes C (1994) Social learning in animals: categories and mechanism. Biol Rev 69:207–231

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

  • Imwalle D, Scordalakales E, Rissman E (2002) Estrogen receptor α influences socially motivated behaviors. Horm Behav 42:484–491

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Lonsdorf E (2016) Sex differences in nonhuman primate behavioral development. J Neurosci Res 95(1–2):213–221

    Google Scholar 

  • Lonstein J, Gammie S (2002) Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev 26(8):869–888

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • MacDougall-Shackleton S, Ball G (1999) Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci 22(10):432–436

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Miczek K, Maxson S, Fish E, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125(1-2):167–181

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson R, Trainor B (2007) Neural mechanisms of aggression. Nat Rev Neurosci 8:536–546

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Olivier B (2005) Serotonergic mechanisms in aggression. Novartis Found Symp 268:171–183

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Patchev A, Gotz F, Rohde W (2004) Differential role of estrogen receptor isoforms in sex-specific brain organization. FASEB J 18:1568–1570

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Potegal M, Ferris C (1989) Intraspecific aggression in male hamsters is inhibited by intrahypothalamic vasopressin-receptor antagonist. Aggress Behav 15(4):311–320

    Google Scholar 

  • Raynaud JP (1973) Influence of rat estradiol binding plasma protein (EBP) on uterotrophic activity. Steroids 21(2):249–258

    CAS  PubMed  Google Scholar 

  • Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11(11):1327–1334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosell D, Siever L (2015) The neurobiology of aggression and violence. CNS Spectr 20(3):254–279

    PubMed  Google Scholar 

  • Rosvall K (2011) Intrasexual competition in females: evidence for sexual selection? Behav Ecol 22(6):1131–1140

    PubMed  PubMed Central  Google Scholar 

  • Rowell T (1970) Baboon menstrual cycles affected by social environment. J Reprod Fertil 21:133–141

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Sawyer T, Hengehold A, Perez W (1984) Chemosensory and hormonal mediation of social memory in male rats. Behav Neurosci 98:908–913

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Silk J (2007) The adaptive value of sociality in mammalian groups. Philos Trans R Soc Lond B Biol Sci 362:539–559

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Soma K, Scotti M, Newman A, Charlier T, Demas G (2008) Novel mechanisms for neuroendocrine regulation of aggression. Front Neuroendocrinol 29(4):476–489

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Spiteri T, Agmo A (2009) Ovarian hormones modulate social recognition in female rats. Physiol Behav 98(1-2):247–250

    CAS  PubMed  Google Scholar 

  • Stoop R (2012) Neuromodulation by oxytocin and vasopressin. Neuron 76(1):142–159

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Vivanti G, Nuske H (2017) Autism, attachment, and social learning: three challenges and a way forward. Behav Brain Res 325:251–259

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wharton A (2009) The sociology of gender: an introduction to theory and research. Wiley

    Google Scholar 

  • Whiten A, van de Waal E (2018) The pervasive role of social learning in primate lifetime development. Behav Ecol Sociobiol 72:80

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wranghama R (2017) Two types of aggression in human evolution. Proc Natl Acad Sci U S A 115(2):245–253

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

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Paletta, P., Bass, N., Aspesi, D., Choleris, E. (2022). Sex Differences in Social Cognition. In: Gibson, C., Galea, L.A.M. (eds) Sex Differences in Brain Function and Dysfunction. Current Topics in Behavioral Neurosciences, vol 62. Springer, Cham. https://doi.org/10.1007/7854_2022_325

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