Pair Bond Hypothesis Statement

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  • Papers of particular interest, published within the period of review, have been highlighted as:

    • of special interest

    •• of outstanding interest

    1. Hofmann HA, Beery AK, Blumstein DT, Couzin ID, Earley RL, Hayes LD, Hurd PL, Lacey EA, Phelps SM, Solomon NG, et al. An evolutionary framework for studying mechanisms of social behavior. Trends Ecol Evol. 2014;29:581–589.[PubMed]

    2•. Sun P, Smith AS, Lei K, Liu Y, Wang Z. Breaking bonds in male prairie vole: long-term effects on emotional and social behavior, physiology, and neurochemistry. Behav Brain Res. 2014;265:22–31.[PubMed] The authors investigate affiliative, anxiety-like, and depressive-like behaviors, circulating stress hormone levels, and neuroplastic changes in the OT, AVP, DA, and CRF systems following partner loss. They find that loss of a bonded partner substantially impacts circulating stress hormones, neural plasticity in neuropeptide systems, and depressive-like and anxiety-like behavior.

    3. Bosch OJ, Nair HP, Ahern TH, Neumann ID, Young LJ. The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology. 2009;34:1406–1415.[PMC free article][PubMed]

    4. McGraw LA, Young LJ. The prairie vole: an emerging model organism for understanding the social brain. Trends Neurosci. 2010;33:103–109.[PMC free article][PubMed]

    5. Garrison JL, Macosko EZ, Bernstein S, Pokala N, Albrecht DR, Bargmann CI. Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. Science. 2012;338:540–543.[PMC free article][PubMed]

    6. Albers HE. Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network. Front Neuroendocrinol. 2014[PMC free article][PubMed]

    7. Anacker AMJ, Beery AK. Life in groups: the roles of oxytocin in mammalian sociality. Front Behav Neurosci. 2013:7. article number (185) [PMC free article][PubMed]

    8. O’Connell LA, Hofmann HA. Evolution of a vertebrate social decision-making network. Science. 2012;336:1154–1157.[PubMed]

    9. Knobloch HS, Grinevich V. Evolution of oxytocin pathways in the brain of vertebrates. Front Behav Neurosci. 2014;8:31.[PMC free article][PubMed]

    10. Young KA, Gobrogge KL, Liu Y, Wang Z. The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrinol. 2011;32:53–69.[PMC free article][PubMed]

    11•. Barrett CE, Keebaugh AC, Ahern TH, Bass CE, Terwilliger EF, Young LJ. Variation in vasopressin receptor (Avpr1a) expression creates diversity in behaviors related to monogamy in prairie voles. Horm Behav. 2013;63:518–526.[PubMed] Using site-specific RNA knockdown, the authors manipulate local levels of AVPR1a expression within the range of naturally occurring variation and establish a causal link between AVPR1a expression levels in the ventral pallidum and variation in social behavior in prairie voles.

    12. Turner LM, Young AR, Rompler H, Schoneberg T, Phelps SM, Hoekstra HE. Monogamy evolves through multiple mechanisms: evidence from V1aR in deer mice. Mol Biol Evol. 2010;27:1269–1278.[PubMed]

    13. Freeman SM, Walum H, Inoue K, Smith AL, Goodman MM, Bales KL, Young LJ. Neuroanatomical distribution of oxytocin and vasopressin 1a receptors in the socially monogamous coppery titi monkey (Callicebus cupreus) Neuroscience. 2014;273:12–23.[PMC free article][PubMed]

    14••. Freeman SM, Inoue K, Smith AL, Goodman MM, Young LJ. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta) Psychoneuroendocrinology. 2014;45:128–141.[PubMed] The authors show that OTR expression in the rhesus macaque is localized to brain areas implicated in visual and auditory processing, which in this species, as in humans, are two primary sensory modalities used for processing social information.

    15. Smith AL, Freeman SM, Stehouwer JS, Inoue K, Voll RJ, Young LJ, Goodman MM. Synthesis and evaluation of C-11, F-18 and I-125 small molecule radioligands for detecting oxytocin receptors. Bioorg Med Chem. 2012;20:2721–2738.[PMC free article][PubMed]

    16. Loup F, Tribollet E, Duboisdauphin M, Dreifuss JJ. Localization of high-affinity binding-sites for oxytocin and vasopressin in the human brain — an autoradiographic study. Brain Res. 1991;555:220–232.[PubMed]

    17. Lieberwirth C, Wang Z. Social bonding: regulation by neuropeptides. Front Neurosci. 2014;8:171.[PMC free article][PubMed]

    18. Oldfield RG, Hofmann HA. Neuropeptide regulation of social behavior in a monogamous cichlid fish. Physiol Behav. 2011;102:296–303.[PubMed]

    19. Romero T, Nagasawa M, Mogi K, Hasegawa T, Kikusui T. Oxytocin promotes social bonding in dogs. Proc Natl Acad Sci USA. 2014;111:9085–9090.[PMC free article][PubMed]

    20. Klatt JD, Goodson JL. Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird. Proc Biol Sci. 2013;280:20122396.[PMC free article][PubMed]

    21•. Kelly AM, Goodson JL. Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches. Proc Natl Acad Sci USA. 2014;111:6069–6074.[PubMed] Using neuroanatomically specific RNA knockdown of the avian OT and AVP homologs, the authors show that hypothalamic AVP and OT are important for numerous aspects of social behavior in the monogamous zebra finch, and suggest evolutionarily conserved roles for these non-oapeptides in modulating social behavior across amniotes, from rodents to birds.

    22. Pedersen A, Tomaszycki ML. Oxytocin antagonist treatments alter the formation of pair relationships in zebra finches of both sexes. Horm Behav. 2012;62:113–119.[PubMed]

    23. Cavanaugh J, Mustoe AC, Taylor JH, French JA. Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers. Psychoneuroendocrinology. 2014;49:1–10.[PMC free article][PubMed]

    24. Smith AS, Agmo A, Birnie AK, French JA. Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata. Horm Behav. 2010;57:255–262.[PMC free article][PubMed]

    25. Jarcho MR, Mendoza SP, Mason WA, Yang X, Bales KL. Intranasal vasopressin affects pair bonding and peripheral gene expression in male Callicebus cupreus. Genes Brain Behav. 2011;10:375–383.[PMC free article][PubMed]

    26. Walum H, Lichtenstein P, Neiderhiser JM, Reiss D, Ganiban JM, Spotts EL, Pedersen NL, Anckarsater H, Larsson H, Westberg L. Variation in the oxytocin receptor gene is associated with pair-bonding and social behavior. Biol Psychiatry. 2012;71:419–426.[PMC free article][PubMed]

    27. Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W, Ganiban JM, Spotts EL, Pedersen NL, Eriksson E, et al. Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci U S A. 2008;105:14153–14156.[PMC free article][PubMed]

    28. Schneiderman I, Zagoory-Sharon O, Leckman JF, Feldman R. Oxytocin during the initial stages of romantic attachment: relations to couples’ interactive reciprocity. Psychoneuroendocrinology. 2012;37:1277–1285.[PMC free article][PubMed]

    29••. Scheele D, Wille A, Kendrick KM, Stoffel-Wagner B, Becker B, Gunturkun O, Maier W, Hurlemann R. Oxytocin enhances brain reward system responses in men viewing the face of their female partner. Proc Natl Acad Sci USA. 2013;110:20308–20313.[PubMed] The authors demonstrate that OT modulates both behavior and neural activity in pair-bonded human males when viewing their partner’s face. Specifically they find that OT enhances neural activation in mesolimbic reward areas, including the NAcc, when viewing a partner’s face, but not an unfamiliar female’s face, suggesting that there may be evolutionarily conserved neuroendocrine mechanisms contributing to human social behavior and cognition.

    30. Scheele D, Striepens N, Gunturkun O, Deutschlander S, Maier W, Kendrick KM, Hurlemann R. Oxytocin modulates social distance between males and females. J Neurosci. 2012;32:16074–16079.[PubMed]

    31. Berridge KC. From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur J Neurosci. 2012;35:1124–1143.[PMC free article][PubMed]

    32. Resendez SL, Aragona BJ. Aversive motivation and the maintenance of monogamous pair bonding. Rev Neurosci. 2013;24:51–60.[PubMed]

    33. Burkett JP, Young LJ. The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction. Psychopharmacology (Berl) 2012;224:1–26.[PMC free article][PubMed]

    34. Banerjee SB, Dias BG, Crews D, Adkins-Regan E. Newly paired zebra finches have higher dopamine levels and immediate early gene Fos expression in dopaminergic neurons. Eur J Neurosci. 2013;38:3731–3739.[PubMed]

    35. Bales KL, Mason WA, Catana C, Cherry SR, Mendoza SP. Neural correlates of pair-bonding in a monogamous primate. Brain Res. 2007;1184:245–253.[PMC free article][PubMed]

    36. Iwasaki M, Poulsen TM, Oka K, Hessler NA. Sexually dimorphic activation of dopaminergic areas depends on affiliation during courtship and pair formation. Front Behav Neurosci. 2014:8.[PMC free article][PubMed]

    37. Young LJ. Oxytocin, social cognition and psychiatry. Neuropsychopharmacology. 2015;40:243–244.[PMC free article][PubMed]

    38••. Skuse DH, Lori A, Cubells JF, Lee I, Conneely KN, Puura K, Lehtimaki T, Binder EB, Young LJ. Common polymorphism in the oxytocin receptor gene (OXTR) is associated with human social recognition skills. Proc Natl Acad Sci USA. 2014;111:1987–1992.[PubMed] OT signaling at its target receptor is known to mediate social olfactory recognition in rodents. Here, the authors show that a human polymorphism in OXTR, the gene encoding OTR, is associated with the ability to recognize faces in humans, suggesting an evolutionarily conserved role of OT in mediating social recognition in rodents and humans across sensory modalities.

    39•. Resendez SL, Dome M, Gormley G, Franco D, Nevarez N, Hamid AA, Aragona BJ. μ-Opioid receptors within subregions of the striatum mediate pair bond formation through parallel yet distinct reward mechanisms. J Neurosci. 2013;33:9140–9149.[PubMed]

    40. Resendez SL, Kuhnmuench M, Krzywosinski T, Aragona BJ. κ-Opioid receptors within the nucleus accumbens shell mediate pair bond maintenance. J Neurosci. 2012;32:6771–6784.[PubMed]

    41. Lim MM, Liu Y, Ryabinin AE, Bai YH, Wang ZX, Young LJ. CRF receptors in the nucleus accumbens modulate partner preference in prairie voles. Hormones Behav. 2007;51:508–515.[PMC free article][PubMed]

    42•. Smith AS, Wang Z. Hypothalamic oxytocin mediates social buffering of the stress response. Biol Psychiatry. 2014;76:281–288.[PubMed] While OT has been implicated in both social behavior and stress, the role of OT release in social contexts on stress response is an emerging area of research. In this study, the effect of a partner’s presence on stress response was investigated in prairie voles. The author’s found that, following stress, presence of the partner reduced circulating levels of stress hormones and inhibited anxiety-like behavior.

    43. Ophir AG, Gessel A, Zheng DJ, Phelps SM. Oxytocin receptor density is associated with male mating tactics and social monogamy. Horm Behav. 2012;61:445–453.[PMC free article][PubMed]

    44. Ophir AG, Wolff JO, Phelps SM. Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc Natl Acad Sci USA. 2008;105:1249–1254.[PMC free article][PubMed]

    45•. Zheng DJ, Larsson B, Phelps SM, Ophir AG. Female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network. Behav Brain Res. 2013;246:139–147.[PubMed] The authors conduct an important study that bridges systems neurobiology and ethology, demonstrating that patterns of nonapeptide receptors across brain networks implicated inreward and social behavior predict mating strategy and reproductive success in female prairie voles.

    46. Rilling JK, Young LJ. The biology of mammalian parenting and its effect on offspring social development. Science. 2014;345:771–776.[PMC free article][PubMed]

    47. Numan M. Neurobiology of Social Behavior: Toward an Understanding of the Prosocial and Antisocial Brain. Academic Press; 2015. pp. 1–345.

    48. Ahern TH, Young LJ. The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster) Front Behav Neurosci. 2009:3.[PMC free article][PubMed]

    49. Barrett CE, Modi ME, Zhang BC, Walum H, Inoue K, Young LJ. Neonatal melanocortin receptor agonist treatment reduces play fighting and promotes adult attachment in prairie voles in a sex-dependent manner. Neuropharmacology. 2014;85:357–366.[PMC free article][PubMed]

    50. Hostetler CM, Harkey SL, Krzywosinski TB, Aragona BJ, Bales KL. Neonatal exposure to the D1 agonist SKF38393 inhibits pair bonding in the adult prairie vole. Behav Pharmacol. 2011;22:703–710.[PMC free article][PubMed]

    51. Bales KL, Perkeybile AM, Conley OG, Lee MH, Guoynes CD, Downing GM, Yun CR, Solomon M, Jacob S, Mendoza SP. Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles. Biol Psychiat. 2013;74:180–188.[PMC free article][PubMed]

    52. Keebaugh AC, Young LJ. Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Horm Behav. 2011;60:498–504.[PMC free article][PubMed]

    53. Yu P, An SC, Tai FD, Zhang X, He FQ, Wang JL, An XL, Wu RY. The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles. Horm Behav. 2012;61:669–677.[PubMed]

    54. Wang H, Duclot F, Liu Y, Wang ZX, Kabbaj M. Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles. Nature Neurosci. 2013;16:919–U184.[PMC free article][PubMed]

    55. Young KA, Gobrogge KL, Wang ZX. The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior. Neurosci Biobehav. 2011;35:498–515.[PMC free article][PubMed]

    56. Young KA, Liu Y, Gobrogge KL, Dietz DM, Wang H, Kabbaj M, Wang ZX. Amphetamine alters behavior and mesocorticolimbic dopamine receptor expression in the monogamous female prairie vole. Brain Res. 2011;1367:213–222.[PMC free article][PubMed]

    57. Young KA, Liu Y, Gobrogge KL, Wang H, Wang ZX. Oxytocin reverses amphetamine-induced deficits in social bonding: evidence for an interaction with nucleus accumbens dopamine. J Neurosci. 2014;34:8499–8506.[PMC free article][PubMed]

    58. Anacker AMJ, Ahern TH, Hostetler CM, Dufour BD, Smith ML, Cocking DL, Li J, Young LJ, Loftis JM, Ryabinin AE. Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles. Proc Natl Acad Sci USA. 2014;111:6052–6057.[PMC free article][PubMed]

    59. Hostetler CM, Anacker AM, Loftis JM, Ryabinin AE. Social housing and alcohol drinking in male–female pairs of prairie voles (Microtus ochrogaster) Psychopharmacology (Berl) 2012;224:121–132.[PMC free article][PubMed]

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