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Conspecific Interactions in Adult Laboratory Rodents: Friends or Foes?

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Social Behavior from Rodents to Humans

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 30))

Abstract

Interactions between adult conspecifics, including sexual behaviors, affiliation, and aggression are crucial for the well-being, survival, and reproduction of mammals. This holds true for any mammalian species, but certainly for humans: An inability to optimally navigate the social system can have a strong negative impact on physical and mental health. Translational rodent models have been used for decades to unravel the neural pathways and substrates involved in normal and abnormal conspecific interactions. Researchers in the field of translational social neuroscience face a double challenge: Not only do they need to pay considerable attention to the behavioral ecology of their model species or their ancestors, they also have to expect a relatively large variability in behavior and adjust their experimental design accordingly. In this chapter, we will lay out traditional and novel rodent models and paradigms to study sexual, affiliative, and aggressive interactions among adult conspecifics. We will discuss the merits and main findings and briefly consider the most promising novel directions. Finally, we review the modulatory involvement of two major players in mammal social interaction: the central oxytocin and vasopressin system.

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References

  • Audero E, Mlinar B, Baccini G, Skachokova ZK, Corradetti R, Gross C (2013) Suppression of serotonin neuron firing increases aggression in mice. J Neurosci Official J Soc Neurosci 33:8678–8688. doi:10.1523/JNEUROSCI.2067-12.2013

    Article  CAS  Google Scholar 

  • Beiderbeck DI, Neumann ID, Veenema AH (2007) Differences in intermale aggression are accompanied by opposite vasopressin release patterns within the septum in rats bred for low and high anxiety. Eur J Neurosci 26(12):3597–3605

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Berdoy M, Drickamer L (2007) Comparative social organization and life history of rattus and mus. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 380–392

    Google Scholar 

  • Blair RJR (2010) Neuroimaging of psychopathy and antisocial behavior: a targeted review. Curr Psychiatry Rep 12:76–82. doi:10.1007/s11920-009-0086-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanchard RJ, Flannelly KJ, Blanchard DC (1988) Life-span studies of dominance and aggression in established colonies of laboratory rats. Physiol Behav 43:1–7. doi:10.1016/0031-9384(88)90089-3

    Article  CAS  PubMed  Google Scholar 

  • Bosch OJ (2013) Maternal aggression in rodents: brain oxytocin and vasopressin mediate pup defence. Philos Trans R Soc Lond B Biol Sci 368(1631):20130085. doi:10.1098/rstb.2013.0085

    Article  PubMed  PubMed Central  Google Scholar 

  • Bromberg-Martin ES, Matsumoto M, Hikosaka O (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68(5):815–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broom M (2002) A unified model of dominance hierarchy formation and maintenance. J Theor Biol 219(1):63–72. doi:10.1006/jtbi.2002.3109

    Article  CAS  PubMed  Google Scholar 

  • Calcagnoli F, Boer S, Althaus M, Boer J, Koolhaas J (2013) Antiaggressive activity of central oxytocin in male rats. Psychopharmacology 229:1–13

    Google Scholar 

  • Caldwell HK, Lee HJ, Macbeth AH, Young WS 3rd (2008) Vasopressin: behavioral roles of an “original” neuropeptide. Prog Neurobiol 84(1):1–24. doi:10.1016/j.pneurobio.2007.10.007

    Article  CAS  PubMed  Google Scholar 

  • Calisi RM, Bentley GE (2009) Lab and field experiments: are they the same animal? Horm Behav 56(1):1–10. doi:10.1016/j.yhbeh.2009.02.010

    Article  PubMed  Google Scholar 

  • Camats Perna J, Engelmann M (2015) Recognizing others: rodent’s social memories. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_413

  • Cases O, Seif I, Grimsby J, Gaspar P, Chen K, Pournin S, Muller U, Aguet M, Babinet C, Shih JC et al (1995) Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268(5218):1763–1766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho MM, DeVries AC, Williams JR, Carter CS (1999) The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113(5):1071–1079

    Article  CAS  PubMed  Google Scholar 

  • Cordero MI, Poirier GL, Marquez C, Veenit V, Fontana X, Salehi B, Ansermet F, Sandi C (2012) Evidence for biological roots in the transgenerational transmission of intimate partner violence. Transl Psychiatry 2:e106. doi:10.1038/tp.2012.32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Boer SF, Caramaschi D, Natarajan D, Koolhaas JM (2009) The vicious cycle towards violence: focus on the negative feedback mechanisms of brain serotonin neurotransmission. Front Behav Neurosci 3:52. doi:10.3389/neuro.08.052.2009

    PubMed  PubMed Central  Google Scholar 

  • de Boer SF, van der Vegt BJ, Koolhaas JM (2003) Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav Genet 33:485–501, doi:10.1023/A:1025766415159

  • de Jong TR, Korosi A, Harris BN, Perea-Rodriguez JP, Saltzman W (2012) Individual variation in paternal responses of virgin male California mice (Peromyscus californicus): behavioral and physiological correlates. Physiol Biochem Zool PBZ 85:740–751. doi:10.1086/665831

    Article  PubMed  Google Scholar 

  • De Jong TR, Harris BN, Perea-Rodriguez JP, Saltzman W (2013) Physiological and neuroendocrine responses to chronic variable stress in male California mice (Peromyscus californicus): influence of social environment and paternal state. Psychoneuroendocrinology 38(10):2023–2033. doi:10.1016/j.psyneuen.2013.03.006

    Article  PubMed  Google Scholar 

  • de Jong TR, Beiderbeck DI, Neumann ID (2014) Measuring virgin female aggression in the female intruder test (FIT): effects of oxytocin, estrous cycle, and anxiety. PLoS ONE 9(3):e91701. doi:10.1371/journal.pone.0091701

    Article  PubMed  PubMed Central  Google Scholar 

  • Desjardins C, Maruniak JA, Bronson FH (1973) Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939–941

    Article  CAS  PubMed  Google Scholar 

  • DeVito LM, Konigsberg R, Lykken C, Sauvage M, Young WS, Eichenbaum H (2009) Vasopressin 1b receptor knock-out impairs memory for temporal order. J Neurosci 29(9):2676–2683. doi:10.1523/jneurosci.5488-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (2013) American Psychiatric Association, Washington, DC

    Google Scholar 

  • Ebner K, Wotjak CT, Landgraf R, Engelmann M (2000) A single social defeat experience selectively stimulates the release of oxytocin, but not vasopressin, within the septal brain area of male rats. Brain Res 872(1–2):87–92

    Article  CAS  PubMed  Google Scholar 

  • Engelmann M, Ebner K, Landgraf R, Holsboer F, Wotjak CT (1999) Emotional stress triggers intrahypothalamic but not peripheral release of oxytocin in male rats. J Neuroendocrinol 11:867–872

    Article  CAS  PubMed  Google Scholar 

  • Feng C, Hackett P, DeMarco A, Chen X, Stair S, Haroon E, Ditzen B, Pagnoni G, Rilling J (2014) Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans. Brain Imaging Behav 1–11. doi:10.1007/s11682-014-9333-9

  • Ferris CF, Delville Y (1994) Vasopressin and serotonin interactions in the control of agonistic behavior. Psychoneuroendocrinology 19(5–7):593–601

    Article  CAS  PubMed  Google Scholar 

  • Giuliano F, Pfaus J, Srilatha B, Balasubramanian S, Hedlund P, S-i Hisasue, Marson L, Wallen K (2010) Experimental models for the study of female and male sexual function. J Sex Med 7:2970–2995. doi:10.1111/j.1743-6109.2010.01960.x

    Article  PubMed  Google Scholar 

  • Goodson JL (2013) Deconstructing sociality, social evolution and relevant nonapeptide functions. Psychoneuroendocrinology 38(4):465–478

    Article  CAS  PubMed  Google Scholar 

  • Guzman YF, Tronson NC, Jovasevic V, Sato K, Guedea AL, Mizukami H, Nishimori K, Radulovic J (2013) Fear-enhancing effects of septal oxytocin receptors. Nat Neurosci 16:1185–1187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haller J (2014) Neurobiological bases of abnormal aggression and violent behaviour. Springer, Vienna, doi:10.1007/978-3-7091-1268-7

  • Haller J, Bakos N (2002) Stress-induced social avoidance: a new model of stress-induced anxiety? Physiol Behav 77(2–3):327–332

    Article  CAS  PubMed  Google Scholar 

  • Haller J, Halasz J, Mikics E, Kruk MR (2004) Chronic glucocorticoid deficiency-induced abnormal aggression, autonomic hypoarousal, and social deficit in rats. J Neuroendocrinol 16(6):550–557

    Article  CAS  PubMed  Google Scholar 

  • Heinrichs SC, Pich EM, Miczek KA, Britton KT, Koob GF (1992) Corticotropin-releasing factor antagonist reduces emotionality in socially defeated rats via direct neurotropic action. Brain Res 581(2):190–197

    Article  CAS  PubMed  Google Scholar 

  • Hollis F, Kabbaj M (2014) Social defeat as an animal model for depression. ILAR J 55(2):221–232. doi:10.1093/ilar/ilu002

    Article  CAS  PubMed  Google Scholar 

  • Johnson SL, Leedom LJ, Muhtadie L (2012) The dominance behavioral system and psychopathology: evidence from self-report, observational, and biological studies. Psychol Bull 138(4):692–743. doi:10.1037/a0027503

    Article  PubMed  PubMed Central  Google Scholar 

  • Keane B, Parsons S, Smucker BJ, Solomon NG (2014) Length polymorphism at the avpr1a locus is correlated with male reproductive behavior in a natural population of prairie voles (Microtus ochrogaster). Behav Ecol Sociobiol 68(12):1951–1964. doi:10.1007/s00265-014-1801-0

    Article  Google Scholar 

  • Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci 361(1476):2215–2228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kisko TM, Wöhr M, Pellis V, Pellis M (2015) From play to aggression: high-frequency 50-kHz ultrasonic vocalizations as play and appeasement signals in rats. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_432

  • Kohls G, Chevallier C, Troiani V, Schultz RT (2012) Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications. J Neurodev Disord 4(1):10

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai W-S, Ramiro L-LR, Yu HA, Johnston RE (2005) Recognition of familiar individuals in golden hamsters: a new method and functional neuroanatomy. J Neurosci 25(49):11239–11247. doi:10.1523/jneurosci.2124-05.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langgartner D, Füchsl AM, Uschold-Schmidt N, Slattery DA, Reber SO (2015) Chronic subordinate colony housing paradigm: a mouse model to characterize the consequences of insufficient glucocorticoid signalling. Front Psychiatry 6, doi:10.3389/fpsyt.2015.00018

  • Lukas M, Neumann ID (2013) Oxytocin and vasopressin in rodent behaviors related to social dysfunctions in autism spectrum disorders. Behav Brain Res 251:85–94

    Article  CAS  PubMed  Google Scholar 

  • Lukas M, Neumann ID (2014) Social preference and maternal defeat-induced social avoidance in virgin female rats: sex differences in involvement of brain oxytocin and vasopressin. J Neurosci Methods 234:101–107. doi:10.1016/j.jneumeth.2014.03.013

    Article  CAS  PubMed  Google Scholar 

  • Lukas M, Toth I, Reber SO, Slattery DA, Veenema AH, Neumann ID (2011) The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacology 36:2159–2168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malatynska E, Knapp RJ (2005) Dominant-submissive behavior as models of mania and depression. Neurosci Biobehav Rev 29:715–737. doi:10.1016/j.neubiorev.2005.03.014

    Article  PubMed  Google Scholar 

  • Miczek KA (1979) A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology 60(3):253–259

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s00213-013-3008-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mier D, Kirsch P (2015) Social-cognitive deficits in schizophrenia. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_427

  • Mooney SJ, Coen CW, Holmes MM, Beery AK (2015) Region-specific associations between sex, social status, and oxytocin receptor density in the brains of eusocial rodents. Neuroscience 303:261–269. doi:10.1016/j.neuroscience.2015.06.043

    Article  CAS  PubMed  Google Scholar 

  • Morales JC, Cole C, Neumann ID, Langraf R, Young LJ (2004) Vasopressin release in the ventral pallidum during mating in the monogamous male prairie vole. Soc Neurosci Abs 2141

    Google Scholar 

  • Natarajan D, Vries Hd, Saaltink D-J, Boer SFd, Koolhaas JM (2009) Delineation of violence from functional aggression in mice: an ethological approach. Behav Genet 39:73–90. doi:10.1007/s10519-008-9230-3

    Article  PubMed  Google Scholar 

  • Neumann ID, Toschi N, Ohl F, Torner L, Kromer SA (2001) Maternal defence as an emotional stressor in female rats: correlation of neuroendocrine and behavioural parameters and involvement of brain oxytocin. Eur J Neurosci 13(5):1016–1024

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen CA, Boccia ML (2006) Vasopressin interactions with oxytocin in the control of female sexual behavior. Neuroscience 139(3):843–851. doi:10.1016/j.neuroscience.2006.01.002

    Article  CAS  PubMed  Google Scholar 

  • Pfaus JG, Kippin TE, Coria-Avila G (2003) What can animal models tell us about human sexual response? Annu Rev Sex Res 14:1–63. doi:10.1080/10532528.2003.10559810

    PubMed  Google Scholar 

  • Pfaus JG, Kippin TE, Coria-Avila GA, Gelez H, Afonso VM, Ismail N, Parada M (2012) Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance. Arch Sex Behav 41:31–62. doi:10.1007/s10508-012-9935-5

    Article  PubMed  Google Scholar 

  • Pietropaolo S, Crusio WE, D’Amato FR (2015) Treatment approaches in rodent models for autism spectrum disorder. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_433

  • Ramos L, Hicks C, Kevin R, Caminer A, Narlawar R, Kassiou M, McGregor IS (2013) Acute prosocial effects of oxytocin and vasopressin when given alone or in combination with 3,4-methylenedioxymethamphetamine (MDMA, /‘Ecstasy/’) in rats: involvement of the V1A receptor. Neuropsychopharmacology 38:2249–2259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos L, Hicks C, Caminer A, McGregor IS (2014) Inhaled vasopressin increases sociability and reduces body temperature and heart rate in rats. Psychoneuroendocrinology 46:46–51. doi:10.1016/j.psyneuen.2014.04.013

    Article  CAS  PubMed  Google Scholar 

  • Ross HE, Cole CD, Smith Y, Neumann ID, Landgraf R, Murphy AZ, Young LJ (2009) Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 162(4):892–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sala M, Braida D, Lentini D, Busnelli M, Bulgheroni E, Capurro V, Finardi A, Donzelli A, Pattini L, Rubino T, Parolaro D, Nishimori K, Parenti M, Chini B (2011) Pharmacologic rescue of impaired cognitive flexibility, social deficits, increased aggression, and seizure susceptibility in oxytocin receptor null mice: a neurobehavioral model of autism. Biol Psychiatry 69(9):875–882

    Article  CAS  PubMed  Google Scholar 

  • Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16:290–304. doi:10.1038/nrn3918

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JC, Reim D, Boeckers T, Schmeisser MJ (2015) Genetic animal models for autism spectrum disorder. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_407

  • Shimamoto A, DeBold J, Holly E, Miczek K (2011) Blunted accumbal dopamine response to cocaine following chronic social stress in female rats: exploring a link between depression and drug abuse. Psychopharmacology 218(1):271–279. doi:10.1007/s00213-011-2364-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strang S, Park SQ (2016) Human cooperation and its underlying mechanisms. Curr Top Behavioural Neurosci doi:10.1007/7854_2016_445

  • Takahashi A, Quadros IM, Almeida RMMd, Miczek KA (2011) Brain serotonin receptors and transporters: initiation vs. termination of escalated aggression. Psychopharmacology 213:183–212. doi:10.1007/s00213-010-2000-y

    Article  CAS  PubMed  Google Scholar 

  • Toth I, Neumann I (2013) Animal models of social avoidance and social fear. Cell Tissue Res 354(1):107–118. doi:10.1007/s00441-013-1636-4

    Article  PubMed  Google Scholar 

  • Trainor BC, Pride MC, Villalon Landeros R, Knoblauch NW, Takahashi EY, Silva AL, Crean KK (2011) Sex differences in social interaction behavior following social defeat stress in the monogamous California mouse (Peromyscus californicus). PLoS ONE 6(2):e17405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzanoulinou S, Sandi C (2015) The programming of the social brain by stress during childhood and adolescence: From rodents to humans. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_430

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Veening JG, Coolen LM (2014) Neural mechanisms of sexual behavior in the male rat: emphasis on ejaculation-related circuits. Pharmacol Biochem Behav 121:170–183. doi:10.1016/j.pbb.2013.12.017

    Article  CAS  PubMed  Google Scholar 

  • Veening JG, Coolen LM, de Jong TR, Joosten HW, de Boer SF, Koolhaas JM, Olivier B (2005) Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur J Pharmacol 526:226–239. doi:10.1016/j.ejphar.2005.09.041

    Article  CAS  PubMed  Google Scholar 

  • Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci USA 104(42):16681–16684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wöhr M, Engelhardt KA, Seffer D, Sungur AÖ, Schwarting RK (2015) Acoustic communication in rats: effects of social experiences on ultrasonic vocalizations as socio-affective signals. Curr Top Behavioural Neurosci. doi:10.1007/7854_2015_410

  • Wotjak CT, Kubota M, Liebsch G, Montkowski A, Holsboer F, Neumann I, Landgraf R (1996) Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: a novel mechanism of regulating adrenocorticotropic hormone secretion? J Neurosci 16(23):7725–7732

    CAS  PubMed  Google Scholar 

  • Young KA, Gobrogge KL, Liu Y, Wang Z (2011) The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrinol 32(1):53–69. doi:10.1016/j.yfrne.2010.07.006

    Article  PubMed  Google Scholar 

  • Ziporyn T, McClintock MK (1991) Passing as an indicator of social dominance among female wild and domestic norway rats. Behaviour 118:26–41. doi:10.1163/156853991X00184

    Article  Google Scholar 

  • Zoicas I, Slattery DA, Neumann ID (2014) Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum. Neuropsychopharmacology 39(13):3027–3035. doi:10.1038/npp.2014.156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Lukas, M., de Jong, T.R. (2015). Conspecific Interactions in Adult Laboratory Rodents: Friends or Foes?. In: Wöhr, M., Krach, S. (eds) Social Behavior from Rodents to Humans. Current Topics in Behavioral Neurosciences, vol 30. Springer, Cham. https://doi.org/10.1007/7854_2015_428

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