Cited by 70Neuroendocrine regulation and behaviorAttachment and Relationship DynamicsHuman-Animal Interaction Studies

Sex, love and oxytocin: Two metaphors and a molecule

Open access
Carter, C. Sue·2022·Neuroscience & Biobehavioral Reviews

Abstract

Dozens of studies, most conducted in the last four decades, have implicated oxytocin, as well as vasopressin and their receptors, in processes that mediate selective sociality and the consequences of early experience. Oxytocin is critical for the capacity to experience emotional safety and healthy sexuality. Oxytocin also plays a central role in almost every aspect of physical and mental health, including the coordination of sociality and loving relationships with physiological reactions to challenges across the lifespan. Species, including prairie voles, that share with humans the capacity for selective social bonds have been a particularly rich source of insights into the behavioral importance of peptides. The purpose of this historical review is to describe the discovery of a central role for oxytocin in behavioral interactions associated with love, and in the capacity to use sociality to anticipate and cope with challenges across the lifespan - a process that here is called "sociostasis."

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neubiorev.2022.104948

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Whereas the construct of oxytocin has become more precise, the definitions and constructs of evolved nest provision are less established.

    “Whereas the construct of oxytocin has become more precise (Carter, 2022), the definitions and constructs of evolved nest provision are less established.”

    From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Carter, 2022

  • The oxytocinergic system may be a critical feature of emotional safety and healthy sexuality, or the biology of love, providing sociostasis throughout life.

    “The oxytocinergic system may be a critical feature of emotional safety and healthy sexuality, or the biology of love, providing “sociostasis” throughout life (Carter, 2022).”

    From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Carter, 2022

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 156 · Cited by 70

Research works printed but not linked: 129

  1. Abdelwahab LA, Galal OO, Abd El-Rahman SS, El-Brairy AI, Khattab MM, & El-Khatib AS (2021). Targeting the oxytocin system to ameliorate early life depressive-like behaviors in maternally-separated rats. Biological & Pharmaceutical Bulletin. 10.1248/bpb.b21-00247 34349049 · DOI
  2. Altemus M, Deuster PA, Galliven E, Carter CS, & Gold PW (1995). Suppression of hypothalmic-pituitary-adrenal axis responses to stress in lactating women. The Journal of Clinical Endocrinology and Metabolism, 80(10), 2954– 2959. 10.1210/jcem.80.10.7559880 7559880 · DOI
  3. Altemus M, Redwine LS, Leong YM, Frye CA, Porges SW, & Carter CS (2001). Responses to laboratory psychosocial stress in postpartum women. Psychosom Med, 63(5), 814– 821. 11573030
  4. Amico JA, Miedlar JA, Cai H-M, & Vollmer RR (2008). Oxytocin knockout mice: A model for studying stress-related and ingestive behaviours. Progress in Brain Research, 170, 53– 64. 10.1016/S0079-6123(08)00405-6 18655871 · DOI
  5. Antoni FA (2019). Magnocellular Vasopressin and the Mechanism of “Glucocorticoid Escape.” Frontiers in Endocrinology, 10, 422. 10.3389/fendo.2019.00422 31297096 PMC6607413 · DOI · Paper page
  6. Bales KL, & Carter CS (2003). Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav, 44(3), 178– 184. 14609540
  7. Bales KL, Plotsky PM, Young LJ, Lim MM, Grotte N, Ferrer E, & Carter CS (2007). Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors. Neuroscience, 144(1), 38– 45. 10.1016/j.neuroscience.2006.09.009 17055176 PMC1774559 · DOI · Paper page
  8. Bangasser DA, Eck SR, & Ordoñes Sanchez E (2019). Sex differences in stress reactivity in arousal and attention systems. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 44(1), 129– 139. 10.1038/s41386-018-0137-2 30022063 PMC6235989 · DOI
  9. Beach FA (1955). The descent of instinct. Psychological Review, 62(6), 401– 410. 10.1037/h0049138 13273556 · DOI
  10. Beach FA (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. Hormones and Behavior, 7(1), 105– 138. 10.1016/0018-506X(76)90008-8 819345 · DOI
  11. Ben-Ari Y (2018). Oxytocin and Vasopressin, and the GABA Developmental Shift During Labor and Birth: Friends or Foes? Frontiers in Cellular Neuroscience, 12, 254. 10.3389/fncel.2018.00254 30186114 PMC6110879 · DOI
  12. Berendzen KM, & Manoli DS (2022). Rethinking the Architecture of Attachment: New Insights into the Role for Oxytocin Signaling. Affective Science. 10.1007/s42761-022-00142-5 PMC9743890 36519145 · DOI
  13. Berendzen KM, Sharma R, Mandujano MA, Wei Y, Rogers FD, Simmons TC, Seelke AHM, Bond JM, Larios RD, Sherman M, Parthasarathy S, Espineda I, Knoedler JR, Beery A, Bales KL, Shah NM, & Manoli DS (2022). Oxytocin receptor is not required for social attachment in prairie voles (p. 2022.07.22.501192). bioRxiv. 10.1101/2022.07.22.501192 PMC10150797 36708707 · DOI
  14. Bosmans G, Bakermans-Kranenburg MJ, Vervliet B, Verhees MWFT, & van IJzendoorn MH (2020). A learning theory of attachment: Unraveling the black box of attachment development. Neuroscience and Biobehavioral Reviews, 113, 287– 298. 10.1016/j.neubiorev.2020.03.014 32276142 · DOI
  15. Bowlby J (1978). Attachment theory and its therapeutic implications. Adolescent Psychiatry, 6, 5– 33. 742687
  16. Bridges RS (2015). PMC4342279; Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol, 36(Journal Article), 178– 196. 10.1016/j.yfrne.2014.11.007 25500107 PMC4342279 · DOI · Paper page
  17. Brown SL, & Brown RM (2015). Connecting prosocial behavior to improved physical health: Contributions from the neurobiology of parenting. Neuroscience and Biobehavioral Reviews, 55, 1– 17. 10.1016/j.neubiorev.2015.04.004 25907371 · DOI
  18. Burris AS, Banks SM, Carter CS, Davidson JM, & Sherins RJ (1992). A long-term, prospective study of the physiologic and behavioral effects of hormone replacement in untreated hypogonadal men. Journal of Andrology, 13(4), 297– 304. 1399830
  19. Burris AS, Gracely RH, Carter CS, Sherins RJ, & Davidson JM (1991). Testosterone therapy is associated with reduced tactile sensitivity in human males. Hormones and Behavior, 25(2), 195– 205. 10.1016/0018-506x(91)90050-r 2066080 · DOI
  20. Caldwell HK, Aulino EA, Freeman AR, Miller TV, & Witchey SK (2017). Oxytocin and behavior: Lessons from knockout mice. Developmental Neurobiology, 77(2), 190– 201. 10.1002/dneu.22431 27513442 · DOI · Paper page
  21. Carcea I, Caraballo NL, Marlin BJ, Ooyama R, Riceberg JS, Mendoza Navarro JM, Opendak M, Diaz VE, Schuster L, Alvarado Torres MI, Lethin H, Ramos D, Minder J, Mendoza SL, Bair-Marshall CJ, Samadjopoulos GH, Hidema S, Falkner A, Lin D, … Froemke RC (2021). Oxytocin neurons enable social transmission of maternal behaviour. Nature. 10.1038/s41586-021-03814-7 PMC8387235 34381215 · DOI · Paper page
  22. Carter CS (1972). Postcopulatory sexual receptivity in the female hamster: The role of the ovary and adrenal. Hormones and Behavior, 3(3), 261– 265. 10.1016/0018-506x(72)90039-6 4681747 · DOI
  23. Carter CS (1973). Stimuli contributing to the decrement in sexual receptivity of female golden hamsters (Mesocricetus auratus). Animal Behaviour, 21(4), 827– 834. 10.1016/s0003-3472(73)80108-3 4798200 · DOI
  24. Carter CS (1992). Oxytocin and sexual behavior. Neurosci Biobehav Rev, 16(2), 131– 144. 1630727
  25. Carter CS (2017a). The Oxytocin-Vasopressin Pathway in the Context of Love and Fear. Frontiers in Endocrinology, 8, 356. 10.3389/fendo.2017.00356 29312146 PMC5743651 · DOI
  26. Carter CS (2017b). The Role of Oxytocin and Vasopressin in Attachment. Psychodynamic Psychiatry, 45(4), 499– 517. 10.1521/pdps.2017.45.4.499 29244625 · DOI
  27. Carter CS (2022). Oxytocin and love: Myths, metaphors and mysteries. Comprehensive Psychoneuroendocrinology, 9, 100107. 10.1016/j.cpnec.2021.100107 35755926 PMC9216351 · DOI · Paper page
  28. Carter CS, & Altemus M (1997). Integrative functions of lactational hormones in social behavior and stress management. Annals of the New York Academy of Sciences, 807, 164– 174. 10.1111/j.1749-6632.1997.tb51918.x 9071349 · DOI
  29. Carter CS, Altemus M, & Chrousos GP (2001). Neuroendocrine and emotional changes in the post-partum period. Progress in Brain Research, 133, 241– 249. 10.1016/s0079-6123(01)33018-2 11589134 · DOI
  30. Carter CS, & Dantzer R (2022). Love and fear: A special issue. Comprehensive Psychoneuroendocrinology, 11, 100151. 10.1016/j.cpnec.2022.100151 35967926 PMC9363639 · DOI
  31. Carter CS, Kenkel WM, MacLean EL, Wilson SR, Perkeybile AM, Yee JR, Ferris CF, Nazarloo HP, Porges SW, Davis JM, Connelly JJ, & Kingsbury MA (2020). Is Oxytocin “Nature’s Medicine”? Pharmacological Reviews, 72(4), 829– 861. 10.1124/pr.120.019398 32912963 PMC7495339 · DOI · Paper page
  32. Carter CS, & Kingsbury MA (2022). Oxytocin and oxygen: The evolution of a solution to the “stress of life.” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 377(1858), 20210054. 10.1098/rstb.2021.0054 35856299 PMC9272143 · DOI
  33. Carter CS, Lederhendler I, & Kirkpatrick B (1997). The integrative neurobiology of affiliation. Introduction. Ann N Y Acad Sci, 807, xiii– xviii. 9071340
  34. Carter CS, & Perkeybile AM (2018). The Monogamy Paradox: What Do Love and Sex Have to Do With It? 6(202). 10.3389/fevo.2018.00202 PMC6910656 31840025 · DOI
  35. Carter CS, & Porges SW (1974). Ovarian hormones and the duration of sexual receptivity in the female golden hamster. Hormones and Behavior, 5(4), 303– 315. 10.1016/0018-506x(74)90017-8 4477151 · DOI
  36. Carter CS, Witt DM, Manock SR, Adams KA, Bahr JM, & Carlstead K (1989). Hormonal correlates of sexual behavior and ovulation in male-induced and postpartum estrus in female prairie voles. Physiology & Behavior, 46(6), 941– 948. 10.1016/0031-9384(89)90195-9 2699360 · DOI
  37. Champagne FA (2009). Nurturing nature: Social experiences and the brain. J Neuroendocrinol, 21(10), 867– 868. 10.1111/j.1365-2826.2009.01901.x 19686450 · DOI
  38. Champagne FA, & Curley JP (2016). Plasticity of the Maternal Brain Across the Lifespan. New Directions for Child and Adolescent Development, 2016(153), 9– 21. 10.1002/cad.20164 27589495 · DOI
  39. Champagne F, Diorio J, Sharma S, & Meaney MJ (2001). Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A, 98(22), 12736– 12741. 10.1073/pnas.221224598 11606726 PMC60123 · DOI · Paper page
  40. Chen E, Lam PH, Finegood ED, Turiano NA, Mroczek DK, & Miller GE (2021). The balance of giving versus receiving social support and all-cause mortality in a US national sample. Proceedings of the National Academy of Sciences of the United States of America, 118(24), e2024770118. 10.1073/pnas.2024770118 34099550 PMC8214686 · DOI
  41. 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. 10571489
  42. Chrousos GP, & Gold PW (1992). The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. Jama, 267(9), 1244– 1252. 1538563
  43. Crews D (2008). Epigenetics and its implications for behavioral neuroendocrinology. Frontiers in Neuroendocrinology, 29(3), 344– 357. 10.1016/j.yfrne.2008.01.003 18358518 PMC2394853 · DOI
  44. Danoff JS, Connelly JJ, Morris JP, & Perkeybile AM (2021). An epigenetic rheostat of experience: DNA methylation of OXTR as a mechanism of early life allostasis. Comprehensive Psychoneuroendocrinology, 8, 100098. 10.1016/j.cpnec.2021.100098 35757665 PMC9216658 · DOI
  45. Danoff JS, Wroblewski KL, Graves AJ, Quinn GC, Perkeybile AM, Kenkel WM, Lillard TS, Parikh HI, Golino HF, Gregory SG, Carter CS, Bales KL, & Connelly JJ (2021). Genetic, epigenetic, and environmental factors controlling oxytocin receptor gene expression. Clinical Epigenetics, 13(1), 23. 10.1186/s13148-021-01017-5 33516250 PMC7847178 · DOI · Paper page
  46. de Lange A-MG, Kaufmann T, Quintana DS, Winterton A, Andreassen OA, Westlye LT, & Ebmeier KP (2021). Prominent health problems, socioeconomic deprivation, and higher brain age in lonely and isolated individuals: A population-based study. Behavioural Brain Research, 414, 113510. 10.1016/j.bbr.2021.113510 34358570 · DOI
  47. De Vries GJ (2004). Minireview: Sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology, 145(3), 1063– 1068. 10.1210/en.2003-1504 14670982 · DOI · Paper page
  48. DeVries A (2002). Corticotropin-releasing factor induces social preferences in male prairie voles. Psychoneuroendocrinology, 27(6), 705– 714. 10.1016/s0306-4530(01)00073-7 12084663 · DOI · Paper page
  49. DeVries AC, Craft TK, Glasper ER, Neigh GN, & Alexander JK (2007). 2006 Curt P. Richter award winner: Social influences on stress responses and health. Psychoneuroendocrinology, 32(6), 587– 603. 17590276
  50. 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 U S A, 93(21), 11980– 11984. 8876248 PMC38169
  51. Dölen G, & Malenka RC (2014). The emerging role of nucleus accumbens oxytocin in social cognition. Biological Psychiatry, 76(5), 354– 355. 10.1016/j.biopsych.2014.06.009 25103539 · DOI
  52. Donaldson ZR, & Manoli DS (2020). Blueprints for Bonding? New Genetic Tools to Parse the Neural Basis of Pair Bonding in Prairie Voles. Neuroscience, 448, 311. 10.1016/j.neuroscience.2020.08.038 33092783 · DOI
  53. Ellis BJ, & Del Giudice M (2019). Developmental Adaptation to Stress: An Evolutionary Perspective. Annual Review of Psychology, 70, 111– 139. 10.1146/annurev-psych-122216-011732 30125133 · DOI
  54. Ellis BJ, Horn AJ, Carter CS, van IJzendoorn MH, & Bakermans-Kranenburg MJ (2021). Developmental programming of oxytocin through variation in early-life stress: Four meta-analyses and a theoretical reinterpretation. Clinical Psychology Review, 86, 101985. 10.1016/j.cpr.2021.101985 33770582 · DOI
  55. Fahrbach SE, Morrell JI, & Pfaff DW (1986). Effect of varying the duration of pre-test cage habituation on oxytocin induction of short-latency maternal behavior. Physiology & Behavior, 37(1), 135– 139. 10.1016/0031-9384(86)90396-3 3737711 · DOI · Paper page
  56. Feldman R (2021). Social Behavior as a Transdiagnostic Marker of Resilience. Annual Review of Clinical Psychology, 17, 153– 180. 10.1146/annurev-clinpsy-081219-102046 33434055 · DOI
  57. Ferris CF, Meenan DM, Axelson JF, & Albers HE (1986). A vasopressin antagonist can reverse dominant/subordinate behavior in hamsters. Physiol Behav, 38(1), 135– 138. 3786493
  58. Fleming AS, & Rosenblatt JS (1974). Olfactory regulation of maternal behavior in rats. II. Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins. Journal of Comparative and Physiological Psychology, 86(2), 233– 246. 10.1037/h0035936 4590492 · DOI
  59. Gnanadesikan GE, Hammock EAD, Tecot SR, Carter CS, & MacLean EL (2021). Specificity of plasma oxytocin immunoassays: A comparison of commercial assays and sample preparation techniques using oxytocin knockout and wildtype mice. Psychoneuroendocrinology, 132, 105368. 10.1016/j.psyneuen.2021.105368 34364024 PMC8487999 · DOI
  60. Gnanadesikan GE, Hammock EAD, Tecot SR, Lewis RJ, Hart R, Carter CS, & MacLean EL (2022). What are oxytocin assays measuring? Epitope mapping, metabolites, and comparisons of wildtype & knockout mouse urine [Preprint]. Neuroscience. 10.1101/2022.03.03.482682 PMC9807061 35714438 · DOI
  61. Goldstein DS, & Kopin IJ (2007). Evolution of concepts of stress. Stress, 10(2), 109– 120. 17514579
  62. Grant AD, & Erickson EN (2022). Birth, love, and fear: Physiological networks from pregnancy to parenthood. Comprehensive Psychoneuroendocrinology, 100138. 10.1016/j.cpnec.2022.100138 35757173 PMC9227990 · DOI
  63. Grippo AJ, McNeal N, Watanasriyakul WT, Cacioppo S, Scotti M-AL, & Dagner A (2019). Behavioral and cardiovascular consequences of disrupted oxytocin communication in cohabitating pairs of male and female prairie voles. Social Neuroscience, 14(6), 649– 662. 10.1080/17470919.2019.1572031 30658044 PMC6669126 · DOI
  64. Grippo AJ, Pournajafi-Nazarloo H, Sanzenbacher L, Trahanas DM, McNeal N, Clarke DA, Porges SW, & Carter CS (2011). Peripheral oxytocin administration buffers autonomic but not behavioral responses to environmental stressors in isolated prairie voles. Stress, 15(2), 149– 161. 10.3109/10253890.2011.605486 21854168 PMC3397123 · DOI · Paper page
  65. Grippo AJ, Trahanas DM, Zimmerman RR, Porges SW, & Carter CS (2009). Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology, 34(10), 1542– 1553. 19553027 PMC2841348
  66. Harlow HF, & Harlow M (1966). Learning to love. American Scientist, 54(3), 244– 272. 4958465
  67. Harmon AC, Huhman KL, Moore TO, & Albers HE (2002). Oxytocin inhibits aggression in female Syrian hamsters. Journal of Neuroendocrinology, 14(12), 963– 969. 10.1046/j.1365-2826.2002.00863.x 12472877 · DOI
  68. Harris JC, & Carter CS (2013). Therapeutic interventions with oxytocin: Current status and concerns. Journal of the American Academy of Child and Adolescent Psychiatry, 52(10), 998– 1000. 10.1016/j.jaac.2013.08.001 24074464 · DOI
  69. Horn AJ, & Carter CS (2021). Love and longevity: A Social Dependency Hypothesis. Comprehensive Psychoneuroendocrinology, 8, 100088. 10.1016/j.cpnec.2021.100088 35757670 PMC9216627 · DOI
  70. Hostinar CE, Sullivan RM, & Gunnar MR (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: A review of animal models and human studies across development. Psychological Bulletin, 140(1), 256– 282. 10.1037/a0032671 23607429 PMC3844011 · DOI · Paper page
  71. Hrdy SB (2009). Mothers and Others: The Evolutionary Origins of Mutual Understanding. Belknap Press of Harvard University Press.
  72. Hurlemann R, & Grinevich V (2018). Behavioral pharmacology of neuropeptides: Oxytocin. Springer.
  73. Jirikowski GF, Ochs SD, & Caldwell JD (2018). Oxytocin and Steroid Actions. Current Topics in Behavioral Neurosciences, 35, 77– 95. 10.1007/7854_2017_9 28812264 · DOI
  74. Jurek B, & Neumann ID (2018). The Oxytocin Receptor: From Intracellular Signaling to Behavior. Physiological Reviews, 98(3), 1805– 1908. 10.1152/physrev.00031.2017 29897293 · DOI · Paper page
  75. Kenkel W (2020). Birth signalling hormones and the developmental consequences of caesarean delivery. Journal of Neuroendocrinology, n/a(n/a), e12912. 10.1111/jne.12912 33145818 PMC10590550 · DOI
  76. Kenkel WM, Perkeybile A-M, Yee JR, Pournajafi-Nazarloo H, Lillard TS, Ferguson EF, Wroblewski KL, Ferris CF, Carter CS, & Connelly JJ (2019). Behavioral and epigenetic consequences of oxytocin treatment at birth. Science Advances, 5(5), eaav2244. 10.1126/sciadv.aav2244 31049395 PMC6494504 · DOI
  77. Keverne EB, & Kendrick KM (1992). Oxytocin facilitation of maternal behavior in sheep. Ann N Y Acad Sci, 652, 83– 101. 1385685
  78. Kingsbury MA, & Bilbo SD (2019). The inflammatory event of birth: How oxytocin signaling may guide the development of the brain and gastrointestinal system. Front Neuroendocrinol, 55(Journal Article), 100794. 10.1016/j.yfrne.2019.100794 31560883 · DOI
  79. Knobloch HS, & Grinevich V (2014). Evolution of oxytocin pathways in the brain of vertebrates. Frontiers in Behavioral Neuroscience, 8, 31. 10.3389/fnbeh.2014.00031 24592219 PMC3924577 · DOI · Paper page
  80. Lansing SW, French JA, & Lonstein JS (2013). Circulating plasma testosterone during early neonatal life in the socially monogamous and biparental prairie vole (Microtus ochrogaster). Psychoneuroendocrinology, 38(2), 306– 309. 10.1016/j.psyneuen.2012.06.003 22770983 · DOI
  81. Leckman JF, Ponguta LA, Pavarini G, Hein SD, McCarthy MF, Staiti H, Hanöz-Penney S, Rubinstein J, Pruett KD, Yazgan MY, Fallon NS, Hartl FJ, Ziv M, Salah R, Britto PR, Fitzpatrick S, & Panter-Brick C (2021). Love and peace across generations: Biobehavioral systems and global partnerships. Comprehensive Psychoneuroendocrinology, 8, 100092. 10.1016/j.cpnec.2021.100092 35757671 PMC9216554 · DOI
  82. Lehrman DS (1953). A Critique of Konrad Lorenz’s Theory of Instinctive Behavior. The Quarterly Review of Biology, 28(4), 337– 363. 10.1086/399858 13121237 · DOI
  83. Leng G, & Leng RI (2021). Oxytocin: A citation network analysis of 10 000 papers. Journal of Neuroendocrinology, e13014. 10.1111/jne.13014 34328668 · DOI
  84. Levine S (2005). Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology, 30(10), 939– 946. 10.1016/j.psyneuen.2005.03.013 15958281 · DOI · Paper page
  85. Liberzon I, & Young EA (1997). Effects of stress and glucocorticoids on CNS oxytocin receptor binding. Psychoneuroendocrinology, 22(6), 411– 422. 10.1016/s0306-4530(97)00045-0 9364620 · DOI
  86. Lim MM, Wang Z, Olazabal 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. 15201909
  87. Lorenz K (1935). Der Kumpan in der Umwelt des Vogels. Der Artgenosse als auslösendes Moment sozialer Verhaltungsweisen. Journal Für Ornithologie. Beiblatt.(Leipzig).
  88. Lorenz K, Latzke M, & Salzen E (2021). On aggression. Routledge.
  89. Ludwig RJ, & Welch MG (2022). Wired to Connect: The Autonomic Socioemotional Reflex Arc. Frontiers in Psychology, 13. https://www.frontiersin.org/articles/10.3389/fpsyg.2022.841207 PMC9268160 35814106 · DOI
  90. MacLean EL, Wilson SR, Martin WL, Davis JM, Nazarloo HP, & Carter CS (2019). Challenges for measuring oxytocin: The blind men and the elephant? Psychoneuroendocrinology, 107, 225– 231. 10.1016/j.psyneuen.2019.05.018 31163380 PMC6634994 · DOI · Paper page
  91. Morais LH, Golubeva AV, Casey S, Scott KA, Ramos Costa AP, Moloney GM, Dinan TG, & Cryan JF (2021). Early-life oxytocin attenuates the social deficits induced by caesarean-section delivery in the mouse. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology. 10.1038/s41386-021-01040-3 PMC8429532 34040156 · DOI
  92. Moss RL, McCann SM, & Dudley CA (1975). Releasing hormones and sexual behavior. Progress in Brain Research, 42, 37– 46. 10.1016/S0079-6123(08)63639-0 1105666 · DOI
  93. Murgatroyd CA, Hicks-Nelson A, Fink A, Beamer G, Gurel K, Elnady F, Pittet F, & Nephew BC (2016). Effects of Chronic Social Stress and Maternal Intranasal Oxytocin and Vasopressin on Offspring Interferon-γ and Behavior. Frontiers in Endocrinology, 7, 155. 10.3389/fendo.2016.00155 28018290 PMC5155012 · DOI
  94. Murphy MR (1985). History of the Capture and Domestication of the Syrian Golden Hamster (Mesocricetus auratus Waterhouse). In Siegel HI (Ed.), The Hamster: Reproduction and Behavior (pp. 3– 20). Springer US. 10.1007/978-1-4757-0815-8_1 · DOI
  95. Nephew B, & Murgatroyd C (2013). The role of maternal care in shaping CNS function. Neuropeptides, 47(6), 371– 378. 10.1016/j.npep.2013.10.013 24210943 PMC3874801 · DOI
  96. Neumann ID (2002). Involvement of the brain oxytocin system in stress coping: Interactions with the hypothalamo-pituitary-adrenal axis. Prog Brain Res, 139, 147– 162. 12436933
  97. Nishimori K, Young LJ, Guo Q, Wang Z, Insel TR, & Matzuk MM (1996). Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proceedings of the National Academy of Sciences, 93(21), 11699– 11704. PMC38121 8876199
  98. Numan M (2006). Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav Cogn Neurosci Rev, 5(4), 163– 190. 17099111
  99. Parker KJ, & Lee TM (2001). Central Vasopressin Administration Regulates the Onset of Facultative Paternal Behavior in Microtus pennsylvanicus (Meadow Voles). Hormones and Behavior, 39(4), 285– 294. 10.1006/hbeh.2001.1655 11374914 · DOI
  100. Perkeybile AM, & Bales KL (2015). Early rearing experience is associated with vasopressin immunoreactivity but not reactivity to an acute non-social stressor in the prairie vole. Physiology & Behavior, 147, 149– 156. 10.1016/j.physbeh.2015.04.024 25890274 PMC4456194 · DOI
  101. Perkeybile AM, & Bales KL (2017). Intergenerational transmission of sociality: The role of parents in shaping social behavior in monogamous and non-monogamous species. J Exp Biol, 220(Pt 1), 114– 123. 10.1242/jeb.142182 28057834 PMC5278619 · DOI
  102. Pfaff DW, & Baum MJ (2018). Hormone-dependent medial preoptic/lumbar spinal cord/autonomic coordination supporting male sexual behaviors. Molecular and Cellular Endocrinology, 467, 21– 30. 10.1016/j.mce.2017.10.018 29100889 · DOI
  103. Phelps SM, Okhovat M, & Berrio A (2017). Individual Differences in Social Behavior and Cortical Vasopressin Receptor: Genetics, Epigenetics, and Evolution. Frontiers in Neuroscience, 11, 537. 10.3389/fnins.2017.00537 29085274 PMC5649215 · DOI
  104. Quintana DS, & Guastella AJ (2020). An Allostatic Theory of Oxytocin. Trends in Cognitive Sciences, 24(7), 515– 528. 10.1016/j.tics.2020.03.008 32360118 · DOI
  105. Redwine LS, Altemus M, Leong YM, & Carter CS (2001). Lymphocyte responses to stress in postpartum women: Relationship to vagal tone. Psychoneuroendocrinology, 26(3), 241– 251. 10.1016/s0306-4530(00)00049-4 11166487 · DOI
  106. Reis HT, Aron A, Clark MS, & Finkel EJ (2013). Ellen Berscheid, Elaine Hatfield, and the Emergence of Relationship Science. Perspectives on Psychological Science: A Journal of the Association for Psychological Science, 8(5), 558– 572. 10.1177/1745691613497966 26173214 · DOI
  107. Rowold K (2019). What Do Babies Need to Thrive? Changing Interpretations of “Hospitalism” in an International Context, 1900–1945. Social History of Medicine: The Journal of the Society for the Social History of Medicine, 32(4), 799– 818. 10.1093/shm/hkx114 31857744 PMC6913704 · DOI
  108. Sakuma Y, & Pfaff DW (1980). LH-RH in the mesencephalic central grey can potentiate lordosis reflex of female rats. Nature, 283(5747), 566– 567. 10.1038/283566a0 6986562 · DOI
  109. Schulkin J, & Sterling P (2019). Allostasis: A Brain-Centered, Predictive Mode of Physiological Regulation. Trends in Neurosciences, 42(10), 740– 752. 10.1016/j.tins.2019.07.010 31488322 · DOI · Paper page
  110. Selye H (1956). The Stress of Life. McGraw-Hill.
  111. Short RV (1984). Breast feeding. Scientific American, 250(4), 35– 41. 10.1038/scientificamerican0484-35 6729428 · DOI
  112. Stern JM, Weinberg J, & Hennessy MB (2010). From Freud to a Modern Understanding of Behavioral, Physiological, and Brain Development. Developmental Psychobiology, 52(7), 609– 615. 10.1002/dev.20496 20882587 PMC4821214 · DOI
  113. Stevenson JR, McMahon EK, Boner W, & Haussmann MF (2019). Oxytocin administration prevents cellular aging caused by social isolation. Psychoneuroendocrinology, 103, 52– 60. 10.1016/j.psyneuen.2019.01.006 30640038 PMC7476076 · DOI
  114. Stribley JM, & Carter CS (1999). Developmental exposure to vasopressin increases aggression in adult prairie voles. Proc Natl Acad Sci U S A, 96(22), 12601– 12604. 10535968 PMC23008
  115. Tang A, Almas A, Zeytinoglu S, Zeanah CH, Nelson CA, & Fox NA (2021). Long-Term Effects of Institutional Care and Enhanced Attachment Relationships on Close Adolescent Friendships. Child Development, 92(6), 2431– 2446. 10.1111/cdev.13592 33997968 PMC8594286 · DOI
  116. Taylor JH, Walton JC, McCann KE, Norvelle A, Liu Q, Vander Velden JW, Borland JM, Hart M, Jin C, Huhman KL, Cox DN, & Albers HE (2022). CRISPR-Cas9 editing of the arginine-vasopressin V1a receptor produces paradoxical changes in social behavior in Syrian hamsters. Proceedings of the National Academy of Sciences of the United States of America, 119(19), e2121037119. 10.1073/pnas.2121037119 35512092 PMC9171636 · DOI · Paper page
  117. Theofanopoulou C (2021). Reconstructing the evolutionary history of the oxytocin and vasotocin receptor gene family: Insights on whole genome duplication scenarios. Developmental Biology, 479, 99– 106. 10.1016/j.ydbio.2021.07.012 34329619 · DOI
  118. Tomova L, Tye K, & Saxe R (2019). The neuroscience of unmet social needs. Social Neuroscience, 1– 11. 10.1080/17470919.2019.1694580 31729923 · DOI · Paper page
  119. Torday JS (2022). Morphological forms arising from the evolutionary process are topologies. Bio Systems, 214, 104646. 10.1016/j.biosystems.2022.104646 35183679 · DOI
  120. Uvnas Moberg K, Handlin L, Kendall-Tackett K, & Petersson M (2019). Oxytocin is a principal hormone that exerts part of its effects by active fragments. Med Hypotheses, 133, 109394. 10.1016/j.mehy.2019.109394 31525634 · DOI · Paper page
  121. Vuppaladhadiam L, Ehsan C, Akkati M, & Bhargava A (2020). Corticotropin-Releasing Factor Family: A Stress Hormone-Receptor System’s Emerging Role in Mediating Sex-Specific Signaling. Cells, 9(4), E839. 10.3390/cells9040839 PMC7226788 32244319 · DOI
  122. Wang Z, Young LJ, De Vries GJ, & Insel TR (1998). Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res, 119, 483– 499. 10074808
  123. Welch MG, & Ludwig RJ (2017). Calming Cycle Theory and the Co-Regulation of Oxytocin. Psychodynamic Psychiatry, 45(4), 519– 540. 10.1521/pdps.2017.45.4.519 29244620 · DOI
  124. Whitman DC, & Albers HE (1995). Role of oxytocin in the hypothalamic regulation of sexual receptivity in hamsters. Brain Research, 680(1–2), 73– 79. 10.1016/0006-8993(95)00233-g 7663986 · DOI
  125. Williams JR, Catania KC, & Carter CS (1992). Development of partner preferences in female prairie voles (Microtus ochrogaster): The role of social and sexual experience. Horm Behav, 26(3), 339– 349. 1398553
  126. Wilson R (1966). Feminine Forever (First Printing edition). W.H.Allen.
  127. Witt DM, Carter CS, & Lnsel TR (1991). Oxytocin Receptor Binding in Female Prairie Voles: Endogenous and Exogenous Oestradiol Stimulation. Journal of Neuroendocrinology, 3(2), 155– 161. 10.1111/j.13652826.1991.tb00258.x 19215517 · DOI
  128. Witt DM, Carter CS, & Walton DM (1990). Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol Biochem Behav, 37(1), 63– 69. 2263668
  129. Zuloaga DG, Heck AL, De Guzman RM, & Handa RJ (2020). Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses. Biology of Sex Differences, 11(1), 44. 10.1186/s13293-020-00319-2 32727567 PMC7388454 · DOI

Authors
Carter, C. S.
Affiliations
Indiana University Bloomington (US)
Corresponding author
Carter, C. Sue
Venue
Neuroscience & Biobehavioral Reviews
Publisher
Elsevier BV
Published
2022-12
Volume
143
Pages
104948
ISSN
0149-7634 (ISSN-L)
OpenAlex
W4308308742
Cited by
70
References
156
Citations by year
2026: 4 · 2025: 44 · 2024: 7 · 2023: 15
FWCI
2.47
Type
journal article
Language
en
Open access
Locations
  • Neuroscience & Biobehavioral Reviews (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institute of Allergy and Infectious Diseases (R01AI098112)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD075750, R01HD098117)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
Keywords
oxytocin, vasopressin, love, social bonds, Microtus ochrogaster, emotional safety, sexuality, early life experience, coping, social behavior
MeSH terms
Animals, Arvicolinae, Humans, Love, Oxytocin, Social Behavior, Receptors, Oxytocin, Metaphor

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review