Oxytocin receptor and vasopressin receptor 1a genes are respectively associated with emotional and cognitive empathy

Hormones and Behavior

Volumn 67, Issue , 2015, Pages 60-65

  Uzefovsky, F ^a,b   Shalev, I ^c   Israel, S ^a   Edelman, S ^a   Raz, Y ^a   Mankuta, D ^d   Knafo Noam, A ^a   Ebstein, R P ^e  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Arginine vasopressin receptor; Cognitive empathy; Emotional empathy; Gene; Oxytocin receptor

Indexed keywords

DNA; OXYTOCIN; OXYTOCIN RECEPTOR; VASOPRESSIN; VASOPRESSIN V1A RECEPTOR; AVPR1A PROTEIN, HUMAN; OXTR PROTEIN, HUMAN; VASOPRESSIN RECEPTOR;

ADULT; ARTICLE; BEHAVIOR ASSESSMENT; BEHAVIOR GENETICS; COGNITIVE EMPATHY; CONTROLLED STUDY; EMOTIONAL EMPATHY; EMPATHY; EMPATHY QUOTIENT; FEMALE; GENE INTERACTION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HORMONAL REGULATION; HORMONE ACTION; HUMAN; INTERPERSONAL REACTIVITY INDEX; MALE; NEUROTRANSMISSION; OXYTOCIN RECEPTOR GENE; QUESTIONNAIRE MEASURE OF EMOTIONAL EMPATHY; SELF REPORT; SINGLE NUCLEOTIDE POLYMORPHISM; SOCIAL COGNITION; VASOPRESSIN RECEPTOR 1A GENE; YOUNG ADULT; COGNITION; EMOTION; GENETIC POLYMORPHISM; GENETICS; INDIVIDUALITY; PHYSIOLOGY;

ADULT; COGNITION; EMOTIONS; EMPATHY; FEMALE; HUMANS; INDIVIDUALITY; MALE; POLYMORPHISM, GENETIC; RECEPTORS, OXYTOCIN; RECEPTORS, VASOPRESSIN; YOUNG ADULT;

EID: 84919884452     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.11.007     Document Type: Article

References (59)

1. Avinun R., Israel S., Shalev I., Gritsenko I., Bornstein G., Ebstein R.P., Knafo A. AVPR1A variant associated with preschoolers' lower altruistic behavior. PLoS One 2011, 6(9):e25274. 10.1371/journal.pone.0025274.
2. Bachner-Melman R., Dina C., Zohar A.H., Constantini N., Lerer E., Hoch S., Lichtenberg P. AVPR1a and SLC6A4 gene polymorphisms are associated with creative dance performance. PLoS Genet. 2005, 1(3):e42.
3. Bakermans-Kranenburg M.J., van IJzendoorn M.H. Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Soc. Cogn. Affect. Neurosci. 2008, 3(2):128-134. 10.1093/scan/nsn004.
4. Baron-Cohen S., Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J. Autism Dev. Disord. 2004, 34(2):163-175.
5. Baron-Cohen S., Wheelwright S., Hill J., Raste Y., Plumb I. The "Reading the Mind in the Eyes" test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J. Child Psychol. Psychiatry 2001, 42(2):241-251.
6. Batson C., Dyck J., Brandt J., Batson J., Powell A., McMaster M., Griffitt C. Five studies testing two new egoistic alternatives to the empathy-altruism hypothesis. J. Pers. Soc. Psychol. 1988, 55(1):52-77.
7. Bosch O.J., Neumann I.D. Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm. Behav. 2012, 61(3):293-303. 10.1016/j.yhbeh.2011.11.002.
8. Chakrabarti B., Dudbridge F., Kent L., Wheelwright S., Hill-Cawthorne G., Allison C., Baron-Cohen S. Genes related to sex steroids, neural growth, and social-emotional behavior are associated with autistic traits, empathy, and Asperger syndrome. Autism Res. 2009, 2(3):157-177. 10.1002/aur.80.
9. Chang W.H., Lee I.H., Chen K.C., Chi M.H., Chiu N.-T., Yao W.J., Chen P.S. Oxytocin receptor gene rs53576 polymorphism modulates oxytocin-dopamine interaction and neuroticism traits-a SPECT study. Psychoneuroendocrinology 2014, 47(0):212-220. 10.1016/j.psyneuen.2014.05.020.
10. Chen F.S., Kumsta R., von Dawans B., Monakhov M., Ebstein R.P., Heinrichs M. Common oxytocin receptor gene (OXTR) polymorphism and social support interact to reduce stress in humans. Proc. Natl. Acad. Sci. 2011, 108(50):19937-19942. 10.1073/pnas.1113079108.
11. Costa B., Pini S., Gabelloni P., Abelli M., Lari L., Cardini A., Martini C. Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology 2009, 34(10):1506-1514. 10.1016/j.psyneuen.2009.05.006.
12. Cox C.L., Uddin L.Q., Di Martino A., Castellanos F.X., Milham M.P., Kelly C. The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain's intrinsic functional dynamics. Soc. Cogn. Affect. Neurosci. 2011, 10.1093/scan/nsr051.
13. Dantzer R., Koob G.F., Le Moal M. Septal vasopressin modulates social memory in male rats. Brain Res. 1988, 457(1):143-147.
14. Davis M. A multidimensional approach to individual differences in empathy. JSAS Cat. Sel. Doc. Psychol. 1980, 10(4):85.
15. Decety J., Jackson P.L. The functional architecture of human empathy. Behav. Cogn. Neurosci. Rev. 2004, 3(2):71-100.
16. Domes G., Heinrichs M., Michel A., Berger C., Herpertz S.C. Oxytocin improves "mind-reading" in humans. Biol. Psychiatry 2006, 61(6):731-733.
17. Donaldson Z.R., Young L.J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 2008, 322(5903):900-904.
18. Feldman R. Oxytocin and social affiliation in humans. Horm. Behav. 2012, 61(3):380-391. 10.1016/j.yhbeh.2012.01.008.
19. Feldman R., Gordon I., Zagoory-Sharon O. Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: considering stress and affiliation components of human bonding. Dev. Sci. 2011, 14(4):752-761.
20. Ferguson J.N., Young L.J., Insel T.R. The neuroendocrine basis of social recognition. Front. Neuroendocrinol. 2002, 23(2):200-224.
21. Hammock E.A., Young L.J. Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol. Biol. Evol. 2004, 21(6):1057-1063.
22. Hoffman M.L. Empathy and Moral Development: Implications for Caring and Justice 2001, Cambridge University Press.
23. Hurlemann R., Patin A., Onur O.A., Cohen M.X., Baumgartner T., Metzler S., Kendrick K.M. Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J. Neurosci. 2010, 30(14):4999-5007. 10.1523/jneurosci. 5538-09.2010.
24. Israel S., Lerer E., Shalev I., Uzefovsky F., Riebold M., Laiba E., Knafo A. The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task. PLoS One 2009, 4(5):e5535.
25. Kim S.J., Young L.J., Gonen D., Veenstra-VanderWeele J., Courchesne R., Courchesne E., Insel T.R. Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol. Psychiatry 2002, 7(5):503-507.
26. Variation in Empathy: The Interplay of Genetic and Environmental Factors 2013, The Guilford Press, New York. A. Knafo, F. Uzefovsky (Eds.).
27. Knafo A., Israel S., Darvasi A., Bachner-Melman R., Uzefovsky F., Cohen L., Ebstein R.P. Individual differences in allocation of funds in the dictator game associated with length of the arginine vasopressin 1a receptor RS3 promoter region and correlation between RS3 length and hippocampal mRNA. Genes Brain Behav. 2008, 7(3):266-275.
28. Kogan A., Saslow L.R., Impett E.A., Oveis C., Keltner D., Rodrigues Saturn S. Thin-slicing study of the oxytocin receptor (OXTR) gene and the evaluation and expression of the prosocial disposition. Proc. Natl. Acad. Sci. 2011, 108(48):19189-19192. 10.1073/pnas.1112658108.
29. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435(7042):673-676.
30. Lerer E., Levi S., Salomon S., Darvasi A., Yirmiya N., Ebstein R.P. Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition. Mol. Psychiatry 2008, 13(10):980-988.
31. Lucht M.J., Barnow S., Sonnenfeld C., Ulrich I., Grabe H.J., Schroeder W., Rosskopf D. Associations between the oxytocin receptor gene (OXTR) and "mind-reading" in humans-an exploratory study. Nord. J. Psychiatry 2013, 67(1):15-21. 10.3109/08039488.2012.700731.
32. Mehrabian A., Epstein N. A measure of emotional empathy. J. Pers. 1972, 40(4):525-543.
33. Meyer-Lindenberg A., Kolachana B., Gold B., Olsh A., Nicodemus K.K., Mattay V., Weinberger D.R. Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol. Psychiatry 2008, 14(10):968-975.
34. Montag C., Brockmann E.-M., Lehmann A., Müller D.J., Rujescu D., Gallinat J. Association between oxytocin receptor gene polymorphisms and self-rated 'empathic concern' in schizophrenia. PLoS One 2012, 7(12):e51882. 10.1371/journal.pone.0051882.
35. Park J., Willmott M., Vetuz G., Toye C., Kirley A., Hawi Z., Kent L. Evidence that genetic variation in the oxytocin receptor (OXTR) gene influences social cognition in ADHD. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2010, 34(4):697-702. 10.1016/j.pnpbp.2010.03.029.
36. Preston S., de Waal F. Empathy: its ultimate and proximate bases. Behav. Brain Sci. 2003, 25(01):1-20.
37. Rodrigues S.M., Saslow L.R., Garcia N., John O.P., Keltner D. Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc. Natl. Acad. Sci. 2009, 10.1073/pnas.0909579106.
38. Schneiderman I., Zagoory-Sharon O., Leckman J.F., Feldman R. Oxytocin during the initial stages of romantic attachment: relations to couples' interactive reciprocity. Psychoneuroendocrinology 2012, 37(8):1277-1285.
39. Schnell K., Bluschke S., Konradt B., Walter H. Functional relations of empathy and mentalizing: an fMRI study on the neural basis of cognitive empathy. Neuroimage 2011, 54(2):1743-1754. 10.1016/j.neuroimage.2010.08.024.
40. Shamay-Tsoory S.G. The neural bases for empathy. Neuroscientist 2011, 17(1):18-24. 10.1177/1073858410379268.
41. Shamay-Tsoory S.G. Empathic processing: its cognitive and affective dimensions and neuroanatomical basis. The Social Neuroscience of Empathy 2011, 215. J. Decety, W. Ickes (Eds.).
42. Shamay-Tsoory S.G., Aharon-Peretz J. Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 2007, 45(13):3054-3067.
43. Shamay-Tsoory S.G., Tomer R., Goldsher D., Berger B.D., Aharon-Peretz J. Impairment in cognitive and affective empathy in patients with brain lesions: anatomical and cognitive correlates. J. Clin. Exp. Neuropsychol. 2004, 26(8):1113-1127.
44. Shamay-Tsoory S.G., Shur S., Barcai-Goodman L., Medlovich S., Harari H., Levkovitz Y. Dissociation of cognitive from affective components of theory of mind in schizophrenia. Psychiatry Res. 2007, 149(1-3):11-23.
45. Shamay-Tsoory S., Harari H., Szepsenwol O., Levkovitz Y. Neuropsychological evidence of impaired cognitive empathy in euthymic bipolar disorder. J. Neuropsychiatry Clin. Neurosci. 2009, 21(1):59-67.
46. Shamay-Tsoory S.G., Aharon-Peretz J., Perry D. Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 2009, 132(3):617-627. 10.1093/brain/awn279.
47. Tansey K.E., Hill M.J., Cochrane L.E., Gill M., Anney R., Gallagher L. Functionality of promoter microsatellites of arginine vasopressin receptor 1A (AVPR1A): implications for autism. Mol. Autism 2011, 2(1):3.
48. Thibonnier M., Graves M.K., Wagner M.S., Chatelain N., Soubrier F., Corvol P., Jeunemaitre X. Study of V1-vascular vasopressin receptor gene microsatellite polymorphisms in human essential hypertension. J. Mol. Cell. Cardiol. 2000, 32(4):557-564.
49. Tost H., Kolachana B., Hakimi S., Lemaitre H., Verchinski B.A., Mattay V.S., Meyer-Lindenberg A. A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc. Natl. Acad. Sci. 2010, 107(31):13936-13941. 10.1073/pnas.1003296107.
50. Uzefovsky F., Shalev I., Israel S., Knafo A., Ebstein R.P. Vasopressin selectively impairs emotion recognition in men. Psychoneuroendocrinology 2011, 37(4):576-580.
51. Uzefovsky F., Shalev I., Israel S., Edelman S., Raz Y., Perach-Barzilay N., Ebstein R. The dopamine D4 receptor gene shows a gender sensitive association with cognitive empathy: evidence from two independent samples. Emotion 2014, 10.1037/a0036555.
52. Walum H., Westberg L., Henningsson S., Neiderhiser J.M., Reiss D., Igl W., Lichtenstein P. 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(37):14153-14156.
53. Wang J., Qin W., Liu B., Zhou Y., Wang D., Zhang Y., Yu C. Neural mechanisms of oxytocin receptor gene mediating anxiety-related temperament. Brain Struct. Funct. 2013, 1-12. 10.1007/s00429-013-0584-9.
54. Wassink T., Piven J., Vieland V., Pietila J., Goedken R., Folstein S., Sheffield V. Examination of AVPR1a as an autism susceptibility gene. Mol. Psychiatry 2004, 9(10):968-972.
55. Wu N., Li Z., Su Y. The association between oxytocin receptor gene polymorphism (OXTR) and trait empathy. J. Affect. Disord. 2012, 138(3):468-472. 10.1016/j.jad.2012.01.009.
56. Yirmiya N., Rosenberg C., Levi S., Salomon S., Shulman C., Nemanov L., Ebstein R.P. Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills. Mol. Psychiatry 2006, 11(5):488-494.
57. Young L.J., Wang Z. The neurobiology of pair bonding. Nat. Neurosci. 2004, 7(10):1048-1054.
58. Zak P.J., Stanton A.A., Ahmadi S. Oxytocin increases generosity in humans. PLoS One 2007, 2(11):e1128.
59. Zaki J., Ochsner K.N. The neuroscience of empathy: progress, pitfalls and promise. Nat. Neurosci. 2012, 15(5):675-680.