Cumulative risk on the oxytocin receptor gene (OXTR) underpins empathic communication difficulties at the first stages of romantic love

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 10, 2014, Pages 1524-1529

  Schneiderman, Inna ^a   Kanat Maymon, Yaniv ^a   Ebstein, Richard P ^a   Feldman, Ruth ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Bonding; Empathy; Genetic risk; OXTR; Oxytocin; Romantic relationships

Indexed keywords

OXTR PROTEIN, HUMAN; OXYTOCIN RECEPTOR;

ADOLESCENT; ADULT; EMPATHY; FEMALE; GENETIC ASSOCIATION STUDY; GENETICS; GENOTYPE; HUMAN; INTERPERSONAL COMMUNICATION; LOVE; MALE; MENTAL STRESS; PAIR BONDING; SELF REPORT; SINGLE NUCLEOTIDE POLYMORPHISM; YOUNG ADULT;

ADOLESCENT; ADULT; COMMUNICATION; EMPATHY; FEMALE; GENETIC ASSOCIATION STUDIES; GENOTYPE; HUMANS; LOVE; MALE; PAIR BOND; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, OXYTOCIN; SELF REPORT; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 84921497590     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst142     Document Type: Article

References (84)

1. Acevedo, B.P., Aron, A., Fisher, H.E., Brown, L.L. (2011). Neural correlates of long-term intense romantic love. Social Cognitive and Affective Neuroscience, 7, 145-59.
2. Anderson, D.K., Saunders, D.G. (2003). Leaving an abusive partner an empirical review of predictors, the process of leaving, and psychological well-being. Trauma, Violence, & Abuse, 4, 163-91.
3. Apicella, C.L., Cesarini, D., Johannesson, M., et al. (2010). No association between oxytocin receptor (OXTR) gene polymorphisms and experimentally elicited social preferences. PLoS One, 5, e11153.
4. Apter-Levi, Y., Feldman, M., Vakart, A., Ebstein, R.P., Feldman, R. (2013). Impact of maternal depression across the first six years of life on the child's mental health, social engagement, and empathy: the moderating role of oxytocin. American Journal of Psychiatry, 170(10), 1161-68.
5. Aron, A. (2005). Reward, motivation, and emotion systems associated with early-stage intense romantic love. Journal of Neurophysiology, 94, 327-37.
6. Bakermans-Kranenburg, M.J., Van IJzendoorn, M.H. (2008). Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Social Cognitive and Affective Neuroscience, 3, 128-34.
7. Bale, T.L., Davis, A.M., Auger, A.P., Dorsa, D.M., McCarthy, M.M. (2001). CNS regionspecific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. The Journal of Neuroscience, 21, 2546-52.
8. Bales, K.L., Mason, W.A., Catana, C., Cherry, S.R., Mendoza, S.P. (2007). Neural correlates of pair-bonding in a monogamous primate. Brain Research, 1184, 245-53.
9. Bartels, A., Zeki, S. (2000). The neural basis of romantic love. Neuroreport, 11, 3829-34.
10. Bartz, J.A., Zaki, J., Bolger, N., et al. (2010). Oxytocin selectively improves empathic accuracy. Psychological Science, 21, 1426-8.
11. Beck, A.T. (1978). Beck Depression Inventory. San Antonio, TX: Harcourt Brace Jovanovich.
12. Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746-54.
13. Bowlby, J. (1969). Attachment and Loss: Attachment. London: The Hogarth Press and the Institute of Psychoanalysis.
14. Burman, B., Margolin, G. (1992). Analysis of the association between marital relationships and health problems: an interactional perspective. Psychological Bulletin, 112, 39.
15. Burri, A., Heinrichs, M., Schedlowski, M., Kruger, T.H.C. (2008). The acute effects of intranasal oxytocin administration on endocrine and sexual function in males. Psychoneuroendocrinology, 33, 591-600.
16. Campbell, L., Kashy, D.A. (2002). Estimating actor, partner, and interaction effects for dyadic data using PROC MIXED and HLM: a user-friendly guide. Personal Relationships, 9, 327-42.
17. Carter, C.S. (1998). Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology, 23, 779-818.
18. Champagne, F., Diorio, J., Sharma, S., Meaney, M.J. (2001). Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proceedings of the National Academy of Sciences of the United States of America, 98, 12736-41.
19. Chapman, J.M., Cooper, J.D., Todd, J.A., Clayton, D.G. (2003). Detecting disease associations due to linkage disequilibrium using haplotype tags: a class of tests and the determinants of statistical power. Human Heredity, 56, 18-31.
20. Chapman, N.H., Wijsman, E.M. (1998). Genome screens using linkage disequilibrium tests: optimal marker characteristics and feasibility. American Journal of Human Genetics, 63, 1872-85.
21. Clayton, D., Chapman, J., Cooper, J. (2004). Use of unphased multilocus genotype data in indirect association studies. Genetic Epidemiology, 27, 415-28.
22. Cohen, S., Wills, T.A. (1985). Stress, social support, and the buffering hypothesis. Psychological Bulletin, 98, 310-57.
23. Collins, N.L., Feeney, B.C. (2000). A safe haven: an attachment theory perspective on support seeking and caregiving in intimate relationships. Journal of Personality and Social Psychology, 78, 1053-73.
24. Costa, B., Pini, S., Gabelloni, P., et al. (2009). Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology, 34, 1506-14.
25. Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., Heinrichs, M. (2009). Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biological Psychiatry, 65, 728-31.
26. Ditzen, B., Schmidt, S., Strauss, B., Nater, U.M., Ehlert, U., Heinrichs, M. (2008). Adult attachment and social support interact to reduce psychological but not cortisol responses to stress. Journal of Psychosomatic Research, 64, 479-86.
27. Domes, G., Heinrichs, M., Gläscher, J., Büchel, C., Braus, D.F., Herpertz, S.C. (2007). Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biological Psychiatry, 62, 1187-90.
28. Ebstein, R.P., Israel, S., Chew, S.H., Zhong, S., Knafo, A. (2010). Genetics of human social behavior. Neuron, 65, 831-44.
29. Emanuele, E., Politi, P., Bianchi, M., Minoretti, P., Bertona, M., Geroldi, D. (2006). Raised plasma nerve growth factor levels associated with early-stage romantic love. Psychoneuroendocrinology, 31, 288-94.
30. Enns, M.W., Cox, B.J., Clara, I., et al. (2002). Parental bonding and adult psychopathology: results from the US National Comorbidity Survey. Psychological Medicine, 32, 997-1008.
31. Feeney, B.C., Lemay, E.P., Jr (2012). Surviving relationship threats: the role of emotional capital. Personality & Social Psychology Bulletin, 38, 1004-17.
32. Feifel, D., Macdonald, K., Cobb, P., Minassian, A. (2012). Adjunctive intranasal oxytocin improves verbal memory in people with schizophrenia. Schizophrenia Research, 139, 207-10.
33. Feldman, R. (1998). Coding Interactive Behavior. Unpublished manual.
34. Feldman, R. (2012). Oxytocin and social affiliation in humans. Hormones and Behavior, 61, 380-91.
35. Feldman, R., Gordon, I., Influs, M., Gutbir, T., Ebstein, R.P. (2013). Parental oxytocin and early caregiving jointly shape children's oxytocin response and social reciprocity. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 38, 1154-62.
36. Feldman, R., Zagoory-Sharon, O., Weisman, O., et al. (2012). Sensitive parenting is associated with plasma oxytocin and polymorphisms in the OXTR and CD38 genes. Biological Psychiatry, 72, 175-81.
37. Ferguson, J.N., Aldag, J.M., Insel, T.R., Young, L.J. (2001). Oxytocin in the medial amygdala is essential for social recognition in the mouse. The Journal of Neuroscience, 21, 8278-85.
38. Furman, D.J., Chen, M.C., Gotlib, I.H. (2011). Variant in oxytocin receptor gene is associated with amygdala volume. Psychoneuroendocrinology, 36, 891-7.
39. Gauderman, W.J., Murcray, C., Gilliland, F., Conti, D.V. (2007). Testing association between disease and multiple SNPs in a candidate gene. Genetic Epidemiology, 31, 383-95.
40. Gimpl, G., Fahrenholz, F. (2001). The oxytocin receptor system: structure, function, and regulation. Physiological Reviews, 81, 629-83.
41. Gonzaga, G.C., Turner, R.A., Keltner, D., Campos, B., Altemus, M. (2006). Romantic love and sexual desire in close relationships. Emotion (Washington, DC), 6, 163-79.
42. Gottman, J.M., Levenson, R.W. (1992). Marital processes predictive of later dissolution: behavior, physiology, and health. Journal of Personality and Social Psychology, 63, 221-33.
43. Gregory, S.G., Connelly, J.J., Towers, A.J., et al. (2009). Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Medicine, 7, 62.
44. Grewen, K.M. (2005). Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact. Psychosomatic Medicine, 67, 531-8.
45. Heck, R.H., Thomas, S.L., Tabata, L.N. (2010). Multilevel and Longitudinal Modeling with IBM SPSS, 1st edn. Chicago, IL: Routledge Academic.
46. Hollander, E., Bartz, J., Chaplin, W., et al. (2007). Oxytocin increases retention of social cognition in autism. Biological Psychiatry, 61, 498-503.
47. Holt-Lunstad, J., Birmingham, W.A., Light, K.C. (2008). Influence of a 'warm touch' support enhancement intervention among married couples on ambulatory blood pressure, oxytocin, alpha amylase, and cortisol. Psychosomatic Medicine, 70, 976-85.
48. Huber, D., Veinante, P., Stoop, R. (2005). Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science (New York, NY), 308, 245-8.
49. Hurlemann, R., Patin, A., Onur, O.A., et al. (2010). Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. Journal of Neuroscience, 30, 4999-5007.
50. Inoue, H., Yamasue, H., Tochigi, M., et al. (2010). Association between the oxytocin receptor gene and amygdalar volume in healthy adults. Biological Psychiatry, 68, 1066-72.
51. Inoue, T., Kimura, T., Azuma, C., et al. (1994). Structural organization of the human oxytocin receptor gene. The Journal of Biological Chemistry, 269, 32451-6.
52. Insel, T.R., Hulihan, T.J. (1995). A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behavioral Neuroscience, 109, 782-9.
53. Insel, T.R., Young, L.J. (2000). Neuropeptides and the evolution of social behavior. Current Opinion in Neurobiology, 10, 784-9.
54. Israel, S., Lerer, E., Shalev, I., et al. (2009). The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task. PLoS One, 4, e5535.
55. Jacob, S., Brune, C.W., Carter, C.S., Leventhal, B.L., Lord, C., Cook, E.H., Jr (2007). Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism. Neuroscience Letters, 417, 6-9.
56. Jacobson, N.S., Moore, D. (1981). Spouses as observers of the events in their relationship. Journal of Consulting and Clinical Psychology, 49, 269-77.
57. Kaplan, N., Morris, R. (2001). Prospects for association-based fine mapping of a susceptibility gene for a complex disease. Theoretical Population Biology, 60, 181-91.
58. Kawamura, Y., Liu, X., Akiyama, T., et al. (2010). The association between oxytocin receptor gene (OXTR) polymorphisms and affective temperaments, as measured by TEMPS-A. Journal of Affective Disorders, 127, 31-7.
59. Kenny, D.A., Kashy, D.A., Cook, W.L. (2006). Dyadic Data Analysis. New York, NY: Guilford Press.
60. Kim, W., Kim, S., Jeong, J., et al. (2009). Temporal changes in functional magnetic resonance imaging activation of heterosexual couples for visual stimuli of loved partners. Psychiatry Investigation, 6, 19-25.
61. Kogan, A., Saslow, L.R., Impett, E.A., Oveis, C., Keltner, D., Saturn, S.R. (2011). Thinslicing study of the oxytocin receptor (OXTR) gene and the evaluation and expression of the prosocial disposition. Proceedings of the National Academy of Sciences of the United States of America, 108, 19189-92.
62. Lerer, E., Levi, S., Salomon, S., Darvasi, A., Yirmiya, N., Ebstein, R.P. (2007). Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition. Molecular Psychiatry, 13, 980-8.
63. Lorenz, K.Z. (1950). The comparative method in studying innate behavior patterns. Physiological Mechanisms in Animal Behavior. (Society's Symposium IV.). Oxford, England: Academic Press, pp. 221-68.
64. Lyons-Ruth, K. (2008). Contributions of the mother-infant relationship to dissociative, borderline, and conduct symptoms in young adulthood. Infant Mental Health Journal, 29, 203-18.
65. Mah, B.L., Van Ijzendoorn, M.H., Smith, R., Bakermans-Kranenburg, M.J. (2013). Oxytocin in postnatally depressed mothers: its influence on mood and expressed emotion. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 40, 267-72.
66. Marazziti, D., Akiskal, H.S., Rossi, A., Cassano, G.B. (1999). Alteration of the platelet serotonin transporter in romantic love. Psychological Medicine, 29, 741-5.
67. Markman, H.J. (1981). Prediction of marital distress: a 5-year follow-up. Journal of Consulting and Clinical Psychology, 49, 760-2.
68. Meyer-Lindenberg, A., Domes, G., Kirsch, P., Heinrichs, M. (2011). Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nature Reviews. Neuroscience, 12, 524-38.
69. Nagasawa, M., Okabe, S., Mogi, K., Kikusui, T. (2012). Oxytocin and mutual communication in mother-infant bonding. Frontiers in Human Neuroscience, 6, 31. doi:10.3389/ fnhum.2012.00031.
70. Rodrigues, S.M., Saslow, L.R., Garcia, N., John, O.P., Keltner, D. (2009). Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proceedings of the National Academy of Sciences of the United States of America, 106, 21437-41.
71. Schneiderman, I., Zagoory-Sharon, O., Leckman, J.F., Feldman, R. (2012). Oxytocin during the initial stages of romantic attachment: relations to couples' interactive reciprocity. Psychoneuroendocrinology, 37, 1277-85.
72. Schork, N.J., Nath, S.K., Fallin, D., Chakravarti, A. (2000). Linkage disequilibrium analysis of biallelic DNA markers, human quantitative trait loci, and threshold-defined case and control subjects. American Journal of Human Genetics, 67, 1208-18.
73. Singer, T., Snozzi, R., Bird, G., et al. (2008). Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Emotion (Washington, DC), 8, 781-91.
74. Souza, R.P., De Luca, V., Meltzer, H.Y., Lieberman, J.A., Kennedy, J.L. (2010). Schizophrenia severity and clozapine treatment outcome association with oxytocinergic genes. The International Journal of Neuropsychopharmacology, 13, 793-8.
75. Spielberger, C.D., Gorsuch, R.L., Lushene, R. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.
76. Tansey, K.E., Brookes, K.J., Hill, M.J., et al. (2010). Oxytocin receptor (OXTR) does not play a major role in the aetiology of autism: genetic and molecular studies. Neuroscience Letters, 474, 163-7.
77. Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift für Tierpsychologie, 20, 410-33.
78. Tost, H., Kolachana, B., Hakimi, S., et al. (2010). A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proceedings of the National Academy of Sciences of the United States of America, 107, 13936-41.
79. Walum, H., Lichtenstein, P., Neiderhiser, J.M., et al. (2012). Variation in the oxytocin receptor gene is associated with pair-bonding and social behavior. Biological Psychiatry, 71, 419-26.
80. Weisman, O., Feldman, R., Goldstein, A. (2012). Parental and romantic attachment shape brain processing of infant cues. Biological Psychology, 89, 533-8.
81. Williams, J.R., Insel, T.R., Harbaugh, C.R., Carter, C.S. (1994). Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). Journal of Neuroendocrinology, 6, 247-50.
82. Wu, N., Li, Z., Su, Y. (2012). The association between oxytocin receptor gene polymorphism (OXTR) and trait empathy. Journal of Affective Disorders, 138, 468-72.
83. Wu, S., Jia, M., Ruan, Y., et al. (2005). Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biological Psychiatry, 58, 74-7.
84. Young, L.J., Wang, Z. (2004). The neurobiology of pair bonding. Nature Neuroscience, 7, 1048-54.