pp 1-28 | Cite as

Neural Circuits Underlying Rodent Sociality: A Comparative Approach

  • Nicole S. LeeEmail author
  • Annaliese K. BeeryEmail author
Part of the Current Topics in Behavioral Neurosciences book series


All mammals begin life in social groups, but for some species, social relationships persist and develop throughout the course of an individual’s life. Research in multiple rodent species provides evidence of relatively conserved circuitry underlying social behaviors and processes such as social recognition and memory, social reward, and social approach/avoidance. Species exhibiting different complex social behaviors and social systems (such as social monogamy or familiarity preferences) can be characterized in part by when and how they display specific social behaviors. Prairie and meadow voles are closely related species that exhibit similarly selective peer preferences but different mating systems, aiding direct comparison of the mechanisms underlying affiliative behavior. This chapter draws on research in voles as well as other rodents to explore the mechanisms involved in individual social behavior processes, as well as specific complex social patterns. Contrasts between vole species exemplify how the laboratory study of diverse species improves our understanding of the mechanisms underlying social behavior. We identify several additional rodent species whose interesting social structures and available ecological and behavioral field data make them good candidates for study. New techniques and integration across laboratory and field settings will provide exciting opportunities for future mechanistic work in non-model species.


Group living Meadow vole Model species Neural circuits Neuroendocrinology Prairie vole Social behavior Sociality 


  1. Agate RJ, Scott BB, Haripal B, Lois C, Nottebohm F (2009) Transgenic songbirds offer an opportunity to develop a genetic model for vocal learning. Proc Natl Acad Sci 106(42):17963–17967Google Scholar
  2. Anacker AMJ, Beery AK (2013) Life in groups: the roles of oxytocin in mammalian sociality. Front Behav Neurosci 7.
  3. Anacker AMJ, Christensen JD, LaFlamme EM, Grunberg DM, Beery AK (2016a) Septal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles. Psychoneuroendocrinology 68:156–162. Scholar
  4. Anacker AMJ, Reitz KM, Goodwin NL, Beery AK (2016b) Stress impairs new but not established relationships in seasonally social voles. Horm Behav 79:52–57. Scholar
  5. Aragona BJ, Liu Y, Curtis JT, Stephan FK, Wang Z (2003) A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. J Neurosci 23(8):3483–3490Google Scholar
  6. Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, Insel TR, Wang Z (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 9(1):133–139. Scholar
  7. Ardiles A, Ewer J, Acosta ML, Kirkwood A, Martinez A, Ebensperger L et al (2013) Octodon degus (Molina 1782): a model in comparative biology and biomedicine. Cold Spring Harb Protoc 2013(4):312–318. Scholar
  8. Bedford NL, Hoekstra HE (2015) Peromyscus mice as a model for studying natural variation. eLife 4:e06813. Scholar
  9. Beery AK, Kaufer D (2015) Stress, social behavior, and resilience: insights from rodents. Neurobiol Stress 1:116–127. Scholar
  10. Beery AK, Zucker I (2010) Oxytocin and same-sex social behavior in female meadow voles. Neuroscience 169(2):665–673. Scholar
  11. Beery AK, Zucker I (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35(3):565–572. Scholar
  12. Beery AK, Lacey EA, Francis DD (2008a) Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J Comp Neurol 507(6):1847–1859. Scholar
  13. Beery AK, Loo TJ, Zucker I (2008b) Day length and estradiol affect same-sex affiliative behavior in the female meadow vole. Horm Behav 54(1):153–159. Scholar
  14. Beery AK, Vahaba DM, Grunberg DM (2014) Corticotropin-releasing factor receptor densities vary with photoperiod and sociality. Horm Behav 66:779–786. Scholar
  15. Beery AK, Kamal Y, Sobrero R, Hayes LD (2016) Comparative neurobiology and genetics of mammalian social behavior. In: Sociobiology of caviomorph rodents: an integrated view. Wiley Blackwell, HobokenGoogle Scholar
  16. Beery AK, Christensen JD, Lee NS, Blandino KL (2018) Specificity in sociality: mice and prairie voles exhibit different patterns of peer affiliation. Front Behav Neurosci 12.
  17. Beloate LN, Coolen LM (2017) Influences of social reward experience on behavioral responses to drugs of abuse: review of shared and divergent neural plasticity mechanisms for sexual reward and drugs of abuse. Neurosci Biobehav Rev 83:356–372. Scholar
  18. Beloate LN, Omrani A, Adan RA, Webb IC, Coolen LM (2016) Ventral tegmental area dopamine cell activation during male rat sexual behavior regulates neuroplasticity and d-amphetamine cross-sensitization following sex abstinence. J Neurosci 36(38):9949–9961. Scholar
  19. Berdoy M, Drickamer LC (2007) Comparative social organization and life history of Rattus and Mus. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological & evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  20. Bergan JF, Ben-Shaul Y, Dulac C (2014) Sex-specific processing of social cues in the medial amygdala. eLife 3.
  21. Bielsky IF, Young LJ (2004) Oxytocin, vasopressin, and social recognition in mammals. Peptides 25(9):1565–1574. Scholar
  22. Bielsky IF, Hu S-B, Szegda KL, Westphal H, Young LJ (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29(3):483–493. Scholar
  23. Bielsky IF, Hu S-B, Ren X, Terwilliger EF, Young LJ (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47(4):503–513. Scholar
  24. Blumstein DT, Ebensperger LA, Hayes LD, Vásquez RA, Ahern TH, Burger JR et al (2010) Toward an integrative understanding of social behavior: new models and new opportunities. Front Behav Neurosci 4.
  25. Bluthe R-M, Schoenen J, Dantzer R (1990) Androgen-dependent vasopressinergic neurons are involved in social recognition in rats. Brain Res 519(1–2):150–157. Scholar
  26. Boonstra R, Xia X, Pavone L (1993) Mating system of the meadow vole, Microtus pennsylvanicus. Behav Ecol 4(1):83–89. Scholar
  27. Bosch OJ, Nair HP, Ahern TH, Neumann ID, Young LJ (2009) The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology 34(6):1406–1415. Scholar
  28. Brenowitz EA, Zakon HH (2015) Emerging from the bottleneck: benefits of the comparative approach to modern neuroscience. Trends Neurosci 38(5):273–278. Scholar
  29. Broadbent NJ, Squire LR, Clark RE (2004) Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci 101(40):14515–14520. Scholar
  30. Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54(3):265–299Google Scholar
  31. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2(1):51–61. Scholar
  32. Bruce LL, Braford MR (2009) Evolution of the limbic system. In: Squire LR (ed) Encyclopedia of neuroscience, vol 4. Academic Press, OxfordGoogle Scholar
  33. Burgos-Robles A, Kimchi EY, Izadmehr EM, Porzenheim MJ, Ramos-Guasp WA, Nieh EH et al (2017) Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment. Nat Neurosci 20(6):824–835. Scholar
  34. Burkett JP, Andari E, Johnson ZV, Curry DC, de Waal FBM, Young LJ (2016) Oxytocin-dependent consolation behavior in rodents. Science 351(6271):375–378. Scholar
  35. Busher P (2007) Social organization and monogamy in the beaver. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological & evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  36. Calhoun JB (1948) Mortality and movement of brown rats (Rattus norvegicus) in artificially supersaturated populations. J Wildl Manag 12(2):167–172. Scholar
  37. Calhoun JB (1962) The ecology and sociology of the Norway rat (US Public Health Service Publication no. 1008). US Government Printing Office, WashingtonGoogle Scholar
  38. Carter CS, Getz LL (1993) Monogamy and the prairie vole. Sci Am 268(6):100–106Google Scholar
  39. Chalfin L, Dayan M, Levy DR, Austad SN, Miller RA, Iraqi FA et al (2014) Mapping ecologically relevant social behaviours by gene knockout in wild mice. Nat Commun 5:4569. Scholar
  40. Cho MM, Courtney A, 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. Scholar
  41. Clipperton-Allen AE, Lee AW, Reyes A, Devidze N, Phan A, Pfaff DW, Choleris E (2012) Oxytocin, vasopressin and estrogen receptor gene expression in relation to social recognition in female mice. Physiol Behav 105(4):915–924. Scholar
  42. Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21(3):472–492. Scholar
  43. Coen CW, Kalamatianos T, Oosthuizen MK, Poorun R, Faulkes CG, Bennett NC (2015) Sociality and the telencephalic distribution of corticotrophin-releasing factor, urocortin 3, and binding sites for CRF type 1 and type 2 receptors: a comparative study of eusocial naked mole-rats and solitary Cape mole-rats. J Comp Neurol 523(16):2344–2371. Scholar
  44. Colonnello V, Iacobucci P, Fuchs T, Newberry RC, Panksepp J (2011) Octodon degus. A useful animal model for social-affective neuroscience research: basic description of separation distress, social attachments and play. Neurosci Biobehav Rev 35(9):1854–1863. Scholar
  45. Colpaert FC (1975) The ventromedial hypothalamus and the control of avoidance behavior and aggression: fear hypothesis versus response-suppression theory of limbic system function. Behav Biol 15(1):27–44. Scholar
  46. Curtis J, Stowe J, Wang Z (2003) Differential effects of intraspecific interactions on the striatal dopamine system in social and non-social voles. Neuroscience 118(4):1165–1173. Scholar
  47. Dark J, Zucker I, Wade GN (1983) Photoperiodic regulation of body mass, food intake, and reproduction in meadow voles. Am J Phys Regul Integr Comp Phys 245(3):R334–R338Google Scholar
  48. DeVries AC, Carter CS (1999) Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster). Can J Zool 77(6):885–889. Scholar
  49. DeVries AC, DeVries MB, Taymans SE, Carter CS (1996) The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc Natl Acad Sci 93:11980–11984Google Scholar
  50. DeVries AC, Johnson CL, Carter CS (1997) Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster). Can J Zool 75(2):295–301. Scholar
  51. Dluzen DE, Muraoka S, Engelmann M, Ebner K, Landgraf R (2000) Oxytocin induces preservation of social recognition in male rats by activating α-adrenoceptors of the olfactory bulb. Eur J Neurosci 12(2):760–766. Scholar
  52. Donaldson ZR, Yang S-H, Chan AWS, Young LJ (2009) Production of germline transgenic prairie voles (Microtus ochrogaster) using lentiviral vectors. Biol Reprod 81(6):1189–1195. Scholar
  53. Donaldson ZR, Spiegel L, Young LJ (2010) Central vasopressin V1a receptor activation is independently necessary for both partner preference formation and expression in socially monogamous male prairie voles. Behav Neurosci 124(1):159–163. Scholar
  54. Ebensperger LA, Hurtado MJ, Soto-Gamboa M, Lacey EA, Chang AT (2004) Communal nesting and kinship in degus (Octodon degus). Naturwissenschaften 91(8):391–395. Scholar
  55. Ebensperger LA, Chesh AS, Castro RA, Tolhuysen LO, Quirici V, Burger JR et al (2011a) Burrow limitations and group living in the communally rearing rodent, Octodon degus. J Mammal 92(1):21–30. Scholar
  56. Ebensperger LA, Ramírez-Estrada J, León C, Castro RA, Tolhuysen LO, Sobrero R et al (2011b) Sociality, glucocorticoids and direct fitness in the communally rearing rodent, Octodon degus. Horm Behav 60(4):346–352. Scholar
  57. Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107(1):1–15. Scholar
  58. Everts HG, Koolhaas J (1999) Differential modulation of lateral septal vasopressin receptor blockade in spatial learning, social recognition, and anxiety-related behaviors in rats. Behav Brain Res 99(1):7–16. Scholar
  59. Faulkes CG, Bennett NC (2007) African mole-rats: social and ecological diversity. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological & evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  60. Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25(3):284–288. Scholar
  61. Ferguson JN, Aldag JM, Insel TR, Young LJ (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21(20):8278–8285Google Scholar
  62. Ferguson JN, Young LJ, Insel TR (2002) The neuroendocrine basis of social recognition. Front Neuroendocrinol 23(2):200–224. Scholar
  63. Ferkin MH (1988) The effect of familiarity on social interactions in meadow voles, Microtus pennsylvanicus: a laboratory and field study. Anim Behav 36(6):1816–1822. Scholar
  64. Fleming AS, Anderson V (1987) Affect and nurturance: mechanisms mediating maternal behavior in two female mammals. Prog Neuro-Psychopharmacol Biol Psychiatry 11(2–3):121–127. Scholar
  65. Foltz DW, Hoogland JL (1981) Analysis of the mating system in the black-tailed prairie dog (Cynomys ludovicianus) by likelihood of paternity. J Mammal 62(4):706–712. Scholar
  66. Fulk GW (1976) Notes on the activity, reproduction, and social behavior of Octodon degus. J Mammal 57(3):495–505. Scholar
  67. Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31(7):397–405. Scholar
  68. Getz LL (1962) Aggressive behavior of the meadow and prairie voles. J Mammal 43(3):351–358. Scholar
  69. Getz LL (1972) Social structure and aggressive behavior in a population of Microtus pennsylvanicus. J Mammal 53(2):310–317. Scholar
  70. Getz LL, Carter CS (1996) Prairie-vole partnerships. Am Sci 84(1):56–62Google Scholar
  71. Getz LL, McGuire B, Pizzuto T, Hofmann JE, Frase B (1993) Social organization of the prairie vole (Microtus ochrogaster). J Mammal 74(1):44–58. Scholar
  72. Gheusi G, Bluthé R-M, Goodall G, Dantzer R (1994) Social and individual recognition in rodents: methodological aspects and neurobiological bases. Behav Process 33(1–2):59–87Google Scholar
  73. Gingrich B, Liu Y, Cascio C, Wang Z, Insel TR (2000) Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav Neurosci 114(1):173–183. Scholar
  74. Godin AJ (1977) Wild mammals of New England. Johns Hopkins University Press, BaltimoreGoogle Scholar
  75. Goodwin NL, Lopez SA, Lee NS, Beery AK (2018) Comparative role of reward in long-term peer and mate relationships in voles. Horm Behav.
  76. Grippo AJ, Cushing BS, Carter CS (2007a) Depression-like behavior and stressor-induced neuroendocrine activation in female prairie voles exposed to chronic social isolation. Psychosom Med 69(2):149–157. Scholar
  77. Grippo AJ, Gerena D, Huang J, Kumar N, Shah M, Ughreja R, Carter CS (2007b) Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 32(8–10):966–980. Scholar
  78. Grippo AJ, Lamb DG, Carter CS, Porges SW (2007c) Social isolation disrupts autonomic regulation of the heart and influences negative affective behaviors. Biol Psychiatry 62(10):1162–1170. Scholar
  79. Grippo AJ, Wu KD, Hassan I, Carter CS (2008) Social isolation in prairie voles induces behaviors relevant to negative affect: toward the development of a rodent model focused on co-occurring depression and anxiety. Depress Anxiety 25(6):E17–E26. Scholar
  80. Grossman SP (1972) Aggression, avoidance, and reaction to novel environments in female rats with ventromedial hypothalamic lesions. J Comp Physiol Psychol 78(2):274–283. Scholar
  81. Gubernick DJ, Alberts JR (1987) The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol 101(2):169–177. Scholar
  82. Gubernick DJ, Nordby JC (1993) Mechanisms of sexual fidelity in the monogamous California mouse, Peromyscus californicus. Behav Ecol Sociobiol 32(3):211–219Google Scholar
  83. Hanken J, Sherman PW (1981) Multiple paternity in Belding’s ground squirrel litters. Science 212(4492):351–353. Scholar
  84. Hare JF, Murie JO (2007) Ecology, kinship, and ground squirrel sociality: insights from comparative analyses. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological & evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  85. Hathaway GA, Faykoo-Martinez M, Peragine DE, Mooney SJ, Holmes MM (2016) Subcaste differences in neural activation suggest a prosocial role for oxytocin in eusocial naked mole-rats. Horm Behav 79:1–7. Scholar
  86. Hofmann HA, Beery AK, Blumstein DT, Couzin ID, Earley RL, Hayes LD et al (2014) An evolutionary framework for studying mechanisms of social behavior. Trends Ecol Evol 29(10):581–589. Scholar
  87. Hofmann HA, Renn SCP, Rubenstein DR (2016) Introduction to symposium: new frontiers in the integrative study of animal behavior: nothing in neuroscience makes sense except in light of behavior. Integr Comp Biol 56(6):1192–1196. Scholar
  88. Hölscher C, Jacob W, Mallot HA (2003) Reward modulates neuronal activity in the hippocampus of the rat. Behav Brain Res 142(1):181–191. Scholar
  89. Hoogland JL (1982) Prairie dogs avoid extreme inbreeding. Science 215(4540):1639–1641. Scholar
  90. Hoogland JL (1983) Nepotism and alarm calling in the black-tailed prairie dog (Cynomys ludovicianus). Anim Behav 31(2):472–479Google Scholar
  91. Hoogland JL (1985) Infanticide in prairie dogs: lactating females kill offspring of close kin. Science 230(4729):1037–1040. Scholar
  92. Hoogland JL (2007) Alarm calling, multiple mating, and infanticide among Black-tailed, Gunnison’s, and Utah prairie dogs. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological & evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  93. Hoogland JL (2013) Prairie dogs disperse when all close kin have disappeared. Science 339(6124):1205–1207. Scholar
  94. Hostinar CE, Sullivan RM, Gunnar MR (2014) Psychobiological mechanisms underlying the social buffering of the HPA axis: a review of animal models and human studies across development. Psychol Bull 140(1):256Google Scholar
  95. Ibe CS, Onyeanusi BI, Hambolu JO, Ayo JO (2010) Sexual dimorphism in the whole brain and brainstem morphometry in the African giant pouched rat (Cricetomys gambianus, Waterhouse 1840). Folia Morphol (Warsz) 69(2):69–74Google Scholar
  96. Insel TR (2003) Is social attachment an addictive disorder? Physiol Behav 79(3):351–357. Scholar
  97. Insel TR, Hulihan TJ (1995) A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109(4):782–789. Scholar
  98. Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212(4494):571–573Google Scholar
  99. Jenkins SH, Busher PE (1979) Castor canadensis. Mamm Species 120:1–8Google Scholar
  100. Johnson ZV, Young LJ (2018) Evolutionary diversity as a catalyst for biological discovery. Integr Zool 13:616. Accepted Author ManuscriptCrossRefGoogle Scholar
  101. Kang Y, Zheng B, Shen B, Chen Y, Wang L, Wang J et al (2015) CRISPR/Cas9-mediated Dax1 knockout in the monkey recapitulates human AHC-HH. Hum Mol Genet 24(25):7255–7264. Scholar
  102. Kalamatianos T, Faulkes CG, Oosthuizen MK, Poorun R, Bennett NC, Coen CW (2010) Telencephalic binding sites for oxytocin and social organization: a comparative study of eusocial naked mole-rats and solitary cape mole-rats. J Comp Neurol 518(10):1792–1813. Scholar
  103. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans Biol Sci 361(1476):2215–2228Google Scholar
  104. Kingsley DM, Zhu B, Osoegawa K, De Jong PJ, Schein J, Marra M et al (2004) New genomic tools for molecular studies of evolutionary change in threespine sticklebacks. Behaviour 141(11):1331–1344Google Scholar
  105. Kishi N, Sato K, Sasaki E, Okano H (2014) Common marmoset as a new model animal for neuroscience research and genome editing technology. Develop Growth Differ 56(1):53–62. Scholar
  106. Kogan JH, Frankland PW, Silva AJ (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10(1):47–56Google Scholar
  107. Krakauer JW, Ghazanfar AA, Gomez-Marin A, MacIver MA, Poeppel D (2017) Neuroscience needs behavior: correcting a reductionist bias. Neuron 93(3):480–490. Scholar
  108. Kültz D, Clayton DF, Robinson GE, Albertson C, Carey HV, Cummings ME et al (2013) New frontiers for organismal biology. Bioscience 63(6):464–471. Scholar
  109. Lacey EA (2004) Sociality reduces individual direct fitness in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis). Behav Ecol Sociobiol 56(5):449–457Google Scholar
  110. Lacey EA, Sherman PW (1991) Social organization of naked mole-rat colonies: evidence for divisions of labor. In: The biology of the naked mole-rat, vol 275. Princeton University Press, Princeton, p 336Google Scholar
  111. Lacey EA, Sherman PW (2007) The ecology of sociality in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  112. Lacey EA, Wieczorek JR (2004) Kinship in colonial tuco-tucos: evidence from group composition and population structure. Behav Ecol 15(6):988–996. Scholar
  113. Lacey EA, Braude SH, Wieczorek JR (1997) Burrow sharing by colonial tuco-tucos (Ctenomys sociabilis). J Mammal 78(2):556–562Google Scholar
  114. Lacey EA, Braude SH, Wieczorek JR (1998) Solitary burrow use by adult Patagonian tuco-tucos (Ctenomys haigi). J Mammal 79(3):986–991Google Scholar
  115. Landgraf R, Gerstberger R, Montkowski A, Probst JC, Wotjak CT, Holsboer F, Engelmann M (1995) V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J Neurosci 15(6):4250–4258Google Scholar
  116. Landgraf R, Frank E, Aldag JM, Neumann ID, Sharer CA, Ren X et al (2003) Viral vector-mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and active social behaviour. Eur J Neurosci 18(2):403–411. Scholar
  117. Lebow MA, Chen A (2016) Overshadowed by the amygdala: the bed nucleus of the stria terminalis emerges as key to psychiatric disorders. Mol Psychiatry 21(4):450–463. Scholar
  118. Lee PC (1994) Social structure and evolution. In: Slater PJB, Halliday TR (eds) Behaviour and evolution. Cambridge University Press, CambridgeGoogle Scholar
  119. Li Y, Dulac C (2018) Neural coding of sex-specific social information in the mouse brain. Curr Opin Neurobiol 53:120–130. Scholar
  120. Li Y, Mathis A, Grewe BF, Osterhout JA, Ahanonu B, Schnitzer MJ et al (2017) Neuronal representation of social information in the medial amygdala of awake behaving mice. Cell 171(5):1176–1190.e17. Scholar
  121. Lidicker WZ (1976) Social behaviour and density regulation in house mice living in large enclosures. J Anim Ecol 45(3):677–697. Scholar
  122. Lim M, Young L (2004) Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125(1):35–45. Scholar
  123. Lim MM, Wang Z, Olazábal DE, Ren X, Terwilliger EF, Young LJ (2004) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429(6993):754–757. Scholar
  124. Litvin Y, Murakami G, Pfaff DW (2011) Effects of chronic social defeat on behavioral and neural correlates of sociality: vasopressin, oxytocin and the vasopressinergic V1b receptor. Physiol Behav 103(3–4):393–403. Scholar
  125. Liu Y, Wang Z (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121(3):537–544. Scholar
  126. Liu Y, Curtis JT, Wang Z (2001) Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav Neurosci 115(4):910–919. Scholar
  127. Lloyd JA (1975) Social structure and reproduction in two freely growing populations of house mice (Mus musculus L.). Anim Behav 23:413–424. Scholar
  128. Lukas D, Clutton-Brock T (2012a) Cooperative breeding and monogamy in mammalian societies. Proc R Soc B Biol Sci 279(1736):2151–2156. Scholar
  129. Lukas D, Clutton-Brock T (2012b) Life histories and the evolution of cooperative breeding in mammals. Proc R Soc B Biol Sci 279(1744):4065–4070. Scholar
  130. Lukas D, Clutton-Brock TH (2013) The evolution of social monogamy in mammals. Science 341(6145):526–530. Scholar
  131. 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. Scholar
  132. 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(11):2159–2168. Scholar
  133. Luo X, Li M, Su B (2016) Application of the genome editing tool CRISPR/Cas9 in non-human primates. Zool Res 37(4):241–219. Scholar
  134. MacDonald DW, Mathews F, Berdoy M (1999) The behaviour and ecology of Rattus norvegicus: from opportunism to kamikaze tendencies. In: Singleton GR, Hinds LA, Leirsand H, Zhang Z (eds) Ecologically-based management of rodent pests, ACIAR Monograph No. 59. Australian Centre for International Agricultural Research, Canberra, pp 49–80Google Scholar
  135. MacKintosh JH (1973) Factors affecting the recognition of territory boundaries by mice (Mus musculus). Anim Behav 21(3):464–470. Scholar
  136. Madison DM (1980) Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav Ecol Sociobiol 7(1):65–71Google Scholar
  137. Madison DM, McShea WJ (1987) Seasonal changes in reproductive tolerance, spacing, and social organization in meadow voles: a microtine model. Am Zool 27(3):899–908. Scholar
  138. Madison DM, FitzGerald RW, McShea WJ (1984) Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences for population cycling. Behav Ecol Sociobiol 15(1):9–17Google Scholar
  139. Mateo JM (2010) Self-referent phenotype matching and long-term maintenance of kin recognition. Anim Behav 80(5):929–935. Scholar
  140. McClintock MK, Anisko JJ (1982) Group mating among Norway rats I. Sex differences in the pattern and neuroendocrine consequences of copulation. Anim Behav 30(2):398–409. Scholar
  141. McClintock MK, Anisko JJ, Adler NT (1982) Group mating among Norway rats II. The social dynamics of copulation: competition, cooperation, and mate choice. Anim Behav 30(2):410–425. Scholar
  142. McHenry JA, Otis JM, Rossi MA, Robinson JE, Kosyk O, Miller NW et al (2017) Hormonal gain control of a medial preoptic area social reward circuit. Nat Neurosci 20(3):449–462Google Scholar
  143. McNeal N, Scotti M-AL, Wardwell J, Chandler DL, Bates SL, LaRocca M et al (2014) Disruption of social bonds induces behavioral and physiological dysregulation in male and female prairie voles. Auton Neurosci 180:9–16. Scholar
  144. McShea WJ, Madison DM (1984) Communal nesting between reproductively active females in a spring population of Microtus pennsylvanicus. Can J Zool 62(3):344–346Google Scholar
  145. Michener GR, Murie JO (1983) Black-tailed prairie dog coteries: are they cooperatively breeding units? Am Nat 121(2):266–274Google Scholar
  146. Miller CT, Freiwald WA, Leopold DA, Mitchell JF, Silva AC, Wang X (2016) Marmosets: a neuroscientific model of human social behavior. Neuron 90(2):219–233. Scholar
  147. Mooney SJ, Douglas NR, Holmes MM (2014) Peripheral administration of oxytocin increases social affiliation in the naked mole-rat (Heterocephalus glaber). Horm Behav 65(4):380–385. Scholar
  148. 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. Scholar
  149. 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(1):242–257. Scholar
  150. Niu Y, Shen B, Cui Y, Chen Y, Wang J, Wang L et al (2014) Generation of gene-modified Cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156(4):836–843. Scholar
  151. Nowak RM (1999) Walker’s mammals of the world, 6th edn. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  152. Numan M (2007) Motivational systems and the neural circuitry of maternal behavior in the rat. Dev Psychobiol 49(1):12–21. Scholar
  153. Numan M, Stolzenberg DS (2009) Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol 30(1):46–64. Scholar
  154. O’Connell LA, Hofmann HA (2011a) Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 32(3):320–335. Scholar
  155. O’Connell LA, Hofmann HA (2011b) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519(18):3599–3639. Scholar
  156. O’Connell LA, Hofmann HA (2012) Evolution of a vertebrate social decision-making network. Science 336(6085):1154–1157. Scholar
  157. Ockendon NF, O’Connell LA, Bush SJ, Monzón-Sandoval J, Barnes H, Székely T et al (2016) Optimization of next-generation sequencing transcriptome annotation for species lacking sequenced genomes. Mol Ecol Resour 16(2):446–458. Scholar
  158. Ondrasek NR, Wade A, Burkhard T, Hsu K, Nguyen T, Post J, Zucker I (2015) Environmental modulation of same-sex affiliative behavior in female meadow voles (Microtus pennsylvanicus). Physiol Behav 140:118–126. Scholar
  159. Ophir AG, Phelps SM, Sorin AB, Wolff JO (2007) Morphological, genetic, and behavioral comparisons of two prairie vole populations in the field and laboratory. J Mammal 88(4):989–999. Scholar
  160. Ophir AG, Zheng D-J, Eans S, Phelps SM (2009) Social investigation in a memory task relates to natural variation in septal expression of oxytocin receptor and vasopressin receptor 1a in prairie voles (Microtus ochrogaster). Behav Neurosci 123(5):979Google Scholar
  161. Parker KJ, Lee TM (2003) Female meadow voles (Microtus pennsylvanicus) demonstrate same-sex partner preferences. J Comp Psychol 117(3):283–289. Scholar
  162. Paxinos G, Franklin KB (2012) The mouse brain in stereotaxic coordinates. Elsevier Academic Press, CambridgeGoogle Scholar
  163. Poole TB, Morgan HDR (1973) Differences in aggressive behaviour between male mice (Mus musculus L.) in colonies of different sizes. Anim Behav 21(4):788–795. Scholar
  164. Poole TB, Morgan HDR (1976) Social and territorial behaviour of laboratory mice (Mus musculus L.) in small complex areas. Anim Behav 24(2):476–480. Scholar
  165. Pyter LM, Weil ZM, Nelson RJ (2005) Latitude affects photoperiod-induced changes in immune response in meadow voles (Microtus pennsylvanicus). Can J Zool 83:1271–1278. Scholar
  166. Resendez SL, Kuhnmuench M, Krzywosinski T, Aragona BJ (2012) κ-opioid receptors within the nucleus accumbens shell mediate pair bond maintenance. J Neurosci 32(20):6771–6784. Scholar
  167. Ribble DO (1992) Dispersal in a monogamous rodent, Peromyscus californicus. Ecology 73(3):859–866Google Scholar
  168. Ribble DO, Salvioni M (1990) Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behav Ecol Sociobiol 26(1):9–15. Scholar
  169. Rosen GJ, Vries GJD, Goldman SL, Goldman BD, Forger NG (2007) Distribution of vasopressin in the brain of the eusocial naked mole-rat. J Comp Neurol 500(6):1093–1105. Scholar
  170. Rosenblatt JS, Mayer AD (1995) An analysis of approach/withdrawal processes in the initiation of maternal behavior in the laboratory rat. In: Hood KE, Greenberg G, Tobach E (eds) Research in developmental and comparative psychology, vol. 1. Behavioral development: concepts of approach/withdrawal and integrative levels. Garland Publishing, New York, pp 177–230Google Scholar
  171. Ross HE, Freeman SM, Spiegel LL, Ren X, Terwilliger EF, Young LJ (2009) Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. J Neurosci 29:1312–1318Google Scholar
  172. Ruan C, Zhang Z (2016) Laboratory domestication changed the expression patterns of oxytocin and vasopressin in brains of rats and mice. Anat Sci Int 91(4):358–370. Scholar
  173. Rubenstein DR, Hofmann HA (2015) Editorial overview: the integrative study of animal behavior. Curr Opin Behav Sci 6:v–viii. Scholar
  174. Ruscio MG, Sweeny T, Hazelton J, Suppatkul P, Carter CS (2007) Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles. Horm Behav 51(1):54–61. Scholar
  175. Schmid-Holmes S, Drickamer LC, Robinson AS, Gillie LL (2001) Burrows and burrow-cleaning behavior of house mice (Mus musculus domesticus). Am Midl Nat 146(1):53–62Google Scholar
  176. Schoepf I, Schradin C (2012) Better off alone! Reproductive competition and ecological constraints determine sociality in the African striped mouse (Rhabdomys pumilio). J Anim Ecol 81(3):649–656. Scholar
  177. Schradin C (2005) When to live alone and when to live in groups: ecological determinants of sociality in the African striped mouse (Rhabdomys pumilio, Sparrman, 1784). Belg J Zool 135(Suppl. 1):77–82Google Scholar
  178. Schradin C (2006) Whole-day follows of striped mice (Rhabdomys pumilio), a diurnal murid rodent. J Ethol 24(1):37–43. Scholar
  179. Schradin C, König B, Pillay N (2010) Reproductive competition favours solitary living while ecological constraints impose group-living in African striped mice. J Anim Ecol 79(3):515–521. Scholar
  180. Schradin C, Lindholm AK, Johannesen J, Schoepf I, Yuen C-H, König B, Pillay N (2012) Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio). Mol Ecol 21(3):541–553. Scholar
  181. Schweinfurth MK, Neuenschwander J, Engqvist L, Schneeberger K, Rentsch AK, Gygax M et al (2017) Do female Norway rats form social bonds? Behav Ecol Sociobiol 71:98Google Scholar
  182. Sherman PW (1981) Kinship, demography, and Belding’s ground squirrel nepotism. Behav Ecol Sociobiol 8(4):251–259Google Scholar
  183. Sherman PW (1985) Alarm calls of Belding’s ground squirrels to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17(4):313–323Google Scholar
  184. Sherman PW, Morton ML (1984) Demography of Belding’s ground squirrels. Ecology 65(5):1617–1628. Scholar
  185. Sherman PW, Jarvis JUM, Alexander RD (eds) (1991) The biology of the naked mole-rat. Princeton University Press, PrincetonGoogle Scholar
  186. Smith AS, Wang Z (2014) Hypothalamic oxytocin mediates social buffering of the stress response. Biol Psychiatry 76(4):281–288. Scholar
  187. Smith KS, Tindell AJ, Aldridge JW, Berridge KC (2009) Ventral pallidum roles in reward and motivation. Behav Brain Res 196(2):155–167. Scholar
  188. So N, Franks B, Lim S, Curley JP (2015) A social network approach reveals associations between mouse social dominance and brain gene expression. PLoS One 10(7):e0134509. Scholar
  189. Solomon NG, Jacquot JJ (2002) Characteristics of resident and wandering prairie voles, Microtus ochrogaster. Can J Zool 80(5):951–955. Scholar
  190. Sun P, Smith AS, Lei K, Liu Y, Wang Z (2014) Breaking bonds in male prairie vole: long-term effects on emotional and social behavior, physiology, and neurochemistry. Behav Brain Res 265:22–31. Scholar
  191. Swiech L, Heidenreich M, Banerjee A, Habib N, Li Y, Trombetta J et al (2015) In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat Biotechnol 33(1):102–106. Scholar
  192. Taborsky M, Hofmann HA, Beery AK, Blumstein DT, Hayes LD, Lacey EA et al (2015) Taxon matters: promoting integrative studies of social behavior. Trends Neurosci 38(4):189–191. Scholar
  193. Tamashiro KLK, Nguyen MMN, Sakai RR (2005) Social stress: from rodents to primates. Front Neuroendocrinol 26(1):27–40. Scholar
  194. Tammone MN, Lacey EA, Relva MA (2012) Habitat use by colonial tuco-tucos (Ctenomys sociabilis): specialization, variation, and sociality. J Mammal 93(6):1409–1419. Scholar
  195. Thomas JA, Birney EC (1979) Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav Ecol Sociobiol 5(2):171–186Google Scholar
  196. Timmer M, Sandi C (2010) A role for glucocorticoids in the long-term establishment of a social hierarchy. Psychoneuroendocrinology 35(10):1543–1552. Scholar
  197. Timmer M, Cordero MI, Sevelinges Y, Sandi C (2011) Evidence for a role of oxytocin receptors in the long-term establishment of dominance hierarchies. Neuropsychopharmacology 36(11):2349–2356. Scholar
  198. Trezza V, Campolongo P, Vanderschuren LJMJ (2011) Evaluating the rewarding nature of social interactions in laboratory animals. Dev Cogn Neurosci 1(4):444–458. Scholar
  199. Turner BN, Iverson SL, Severson KL (1983) Seasonal changes in open-field behavior in wild male meadow voles (Microtus pennsylvanicus). Behav Neural Biol 39(1):60–77. Scholar
  200. van der Kooij MA, Sandi C (2012) Social memories in rodents: methods, mechanisms and modulation by stress. Neurosci Biobehav Rev 36(7):1763–1772. Scholar
  201. Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463(1):199–216. Scholar
  202. Wan H, Feng C, Teng F, Yang S, Hu B, Niu Y et al (2015) One-step generation of p53 gene biallelic mutant Cynomolgus monkey via the CRISPR/Cas system. Cell Res 25(2):258Google Scholar
  203. Wang Z, Yu G, Cascio C, Liu Y, Gingrich B, Insel TR (1999) Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): a mechanism for pair bonding? Behav Neurosci 113(3):602Google Scholar
  204. Williams JR, Carter CS, Insel T (1992) Partner preference development in female prairie voles is facilitated by mating or the central infusion of oxytocin. Ann N Y Acad Sci 652(1):487–489. Scholar
  205. Williams JR, Insel TR, Harbaugh CR, Carter CS (1994) Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6(3):247–250. Scholar
  206. Williamson CM, Romeo RD, Curley JP (2017) Dynamic changes in social dominance and mPOA GnRH expression in male mice following social opportunity. Horm Behav 87:80–88. Scholar
  207. Wilsson L (1971) Observations and experiments on the ethology of the European beaver (Castor fiber L.). Viltrevy 8(3):115–266Google Scholar
  208. Winslow JT, Insel TR (2004) Neuroendocrine basis of social recognition. Curr Opin Neurobiol 14(2):248–253. Scholar
  209. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365(6446):545–548Google Scholar
  210. Wolff JO, Sherman PW (2007) Rodent societies: an ecological and evolutionary perspective. The University of Chicago Press, ChicagoGoogle Scholar
  211. Yao S, Bergan J, Lanjuin A, Dulac C (2017) Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues. eLife 6:e31373. Scholar
  212. Young LJ, Murphy Young AZ, Hammock EAD (2005) Anatomy and neurochemistry of the pair bond. J Comp Neurol 493(1):51–57. Scholar
  213. Young KA, Gobrogge KL, Wang Z (2011) The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior. Neurosci Biobehav Rev 35(3):498–515. Scholar
  214. Zegeren KV (1979) Variation in aggressiveness and the regulation of numbers in house mouse populations. Neth J Zool 30(4):635–770. Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Neuroscience and Behavior ProgramUniversity of MassachusettsAmherstUSA
  2. 2.Department of PsychologySmith CollegeNorthamptonUSA
  3. 3.Neuroscience ProgramSmith CollegeNorthamptonUSA

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