Oxytocin gene polymorphisms influence human dopaminergic function in a sex-dependent manner

Biological Psychiatry

Volumn 72, Issue 3, 2012, Pages 198-206

  Love, Tiffany M ^a   Enoch, Mary Anne ^b   Hodgkinson, Colin A ^b   Peciña, Marta ^a   Mickey, Brian ^a,c   Koeppe, Robert A ^d   Stohler, Christian S ^e   Goldman, David ^b   Zubieta, Jon Kar ^a,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Dopamine; genetics; humans; oxytocin; positron emission tomography; sex differences

Indexed keywords

OXYTOCIN; RACLOPRIDE C 11;

ADULT; ALLELE; ANXIETY; ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; DOPAMINERGIC TRANSMISSION; EMOTIONAL ATTACHMENT; EMOTIONAL STRESS; FEMALE; GENETIC DIFFERENCE; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPING TECHNIQUE; HAPLOTYPE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; HUMAN EXPERIMENT; MALE; MYALGIA; NORMAL HUMAN; PAIN ASSESSMENT; PHYSICAL STRESS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PSYCHOLOGICAL WELL BEING; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; ALLELES; ANXIETY; DOPAMINE; EMOTIONS; FEMALE; GENOTYPE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINKAGE DISEQUILIBRIUM; MAGNETIC RESONANCE IMAGING; MALE; OBJECT ATTACHMENT; OXYTOCIN; PAIN; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION;

EID: 84863722826     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.01.033     Document Type: Article

References (100)

1. Ott I, Scott JC (1910): The galactogogue action of the thymus and corpus luteum. Proc Soc Exp Biol Med 8:49-50.
2. Dale HH (1906): On some physiological actions of ergot. J Physiol 34: 163-206.
3. Lee H-J, Macbeth AH, Pagani JH, Young WS (2009): Oxytocin: the great facilitator of life. Prog Neurobiol 88:127-151.
4. Donaldson ZR, Young LJ (2008): Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900-904.
5. Loup F, Tribollet E, Dubois-Dauphin M, Dreifuss JJ (1991): Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res 555:220-232.
6. Caffé AR, Van Ryen PC, Van der Woude TP, Van Leeuwen FW (1989): Vasopressin and oxytocin systems in the brain and upper spinal cord of Macaca fascicularis. J Comp Neuro 287:302-325.
7. Fliers E, Guldenaar SE, van de Wal N, Swaab DF (1986): Extrahypothalamic vasopressin and oxytocin in the human brain; presence of vasopressin cells in the bed nucleus of the stria terminalis. Brain Res 375: 363-367. (Pubitemid 16078056)
8. Jenkins JS, Ang VT, Hawthorn J, Rossor MN (1983): Quantitative distribution of neurohypophysial hormones in human brain and spinal cord. Prog Brain Res 60:123-128.
9. Krémarik P, Freund-Mercier MJ, Stoeckel ME (1993): Histoautoradiographic detection of oxytocin-and vasopressin-binding sites in the telencephalon of the rat. J Comp Neurol 333:343-359. (Pubitemid 23187532)
10. Van Leeuwen FW, van Heerikhuize J, van der Meulen G, Wolters P (1985): Light microscopic autoradiographic localization of [3H]oxytocin binding sites in the rat brain, pituitary and mammary gland. Brain Res 359:320-325. (Pubitemid 16147553)
11. Brinton RE, Wamsley JK, Gee KW, Wan YP, Yamamura HI (1984): [3H]oxytocin binding sites in the rat brain demonstrated by quantitative light microscopic autoradiography. Eur J Pharmacol 102:365-367. (Pubitemid 14096240)
12. Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, Insel TR, et al. (2006): Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 9:133-139. (Pubitemid 43011919)
13. 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 23:3483-3490. (Pubitemid 36531991)
14. Liu Y, Wang ZX (2003): Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121:537-544. (Pubitemid 38367494)
15. 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 114:173-183. (Pubitemid 30131596)
16. Keer SE, Stern JM (1999): Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 67:659-669.
17. Shahrokh DK, Zhang T-Y, Diorio J, Gratton A, Meaney MJ (2010): Oxytocin- dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151:2276-2286.
18. Melis MR, Melis T, Cocco C, Succu S, Sanna F, Pillolla G, et al. (2007): Oxytocin injected into the ventral tegmental area induces penile erection and increases extracellular dopamine in the nucleus accumbens and paraventricular nucleus of the hypothalamus of male rats. Eur J Neurosci 26:1026-1035. (Pubitemid 47274616)
19. Becker JB (2009): Sexual differentiation of motivation: A novel mechanism? Horm Behav 55:646-654.
20. Insel TR (2003): Is social attachment an addictive disorder? Physiol Behav 79:351-357.
21. Lim MM, Young LJ (2006): Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm Behav 50:506-517. (Pubitemid 44307118)
22. Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA (1994): Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108: 1163-1171.
23. Gu X-L, Yu L-C (2007): Involvement of opioid receptors in oxytocin-induced antinociception in the nucleus accumbens of rats. J Pain 8:85-90. (Pubitemid 46026969)
24. Han Y, Yu L-C (2009): Involvement of oxytocin and its receptor in nociceptive modulation in the central nucleus of amygdala of rats. Neurosci Lett 454:101-104.
25. Scott D, Heitzeg M, Koeppe R, Stohler C, Zubieta J (2006): Variations in the human pain stress experience mediated by ventral and dorsal basal ganglia dopamine activity. J Neurosci 26:10789-10795.
26. Kovács GL, Izbéki F, Horváth Z, Telegdy G (1984): Effects of oxytocin and a derivative (Z-prolyl-D-leucine) on morphine tolerance/withdrawal are mediated by the limbic system. Behav Brain Res 14:1-8. (Pubitemid 15191566)
27. Kovács GL, Horváth Z, Sarnyai Z, Faludi M, Telegdy G (1985): Oxytocin and a C-terminal derivative (Z-prolyl-D-leucine) attenuate tolerance to and dependence on morphine and interact with dopaminergic neurotransmission in the mouse brain. Neuropharmacology 24:413-419. (Pubitemid 15096711)
28. Kovàcs GL, Sarnyai Z, Barbarczi E, Szabó G, TelegdyG(1990): The role of oxytocin-dopamine interactions in cocaine-induced locomotor hyperactivity. Neuropharmacology 29:365-368. (Pubitemid 20113896)
29. Kovács GL, Sarnyai Z, SzabóG(1998): Oxytocin and addiction:Areview. Psychoneuroendocrinology 23:945-962.
30. Sarnyai Z, Szabó G, Kovács GL, Telegdy G (1990): Oxytocin attenuates the cocaine-induced exploratory hyperactivity in mice. Neuroreport 1:200-202.
31. Sarnyai Z, Kovács GL (1994): Role of oxytocin in the neuroadaptation to drugs of abuse. Psychoneuroendocrinology 19:85-117. (Pubitemid 24062430)
32. Sarnyai Z (2011): Oxytocin as a potential mediator and modulator of drug addiction. Addict Biol 16:199-201.
33. Pfister HP, Muir JL (1989): Influence of exogenously administered oxytocin on central noradrenaline, dopamine and serotonin levels following psychological stress in nulliparous female rats (Rattus norvegicus). Int J Neurosci 45:221-229.
34. Strathearn L, Li J, Fonagy P, Montague PR (2008): What's in a smile? Maternal brain responses to infant facial cues. Pediatrics 122:40-51.
35. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E (2008): Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58:639-650. (Pubitemid 351672358)
36. Hodgkinson CA, Yuan Q, Xu K, Shen P-H, Heinz E, Lobos EA, et al. (2008): Addictions biology: Haplotype-based analysis for 130 candidate genes on a single array. Alcohol Alcohol 43:505-515.
37. Abi-Dargham A, Rodenhiser J, Printz D, Zea-Ponce Y, Gil R, Kegeles LS, et al. (2000): Increased baseline occupancy of D2 receptors by dopamine in schizophrenia. Proc Natl Acad Sci U S A 97:8104-8109. (Pubitemid 30460780)
38. Souza RP, Ismail P, Meltzer HY, Kennedy JL (2010): Variants in the oxytocin gene and risk for schizophrenia. Schizophr Res 121:279-280.
39. Marazziti D, Dell'Osso B, Baroni S, Mungai F, Catena M, Rucci P, et al. (2006): A relationship between oxytocin and anxiety of romantic attachment. Clin Pract Epidemiol Ment Health 2:28-32.
40. Brennan K, Clark C, Shaver P (1998): Self-report measurement of adult attachment. In: Simpson J, Rholes W, editors. Attachment Theory and Close Relationships. New York: The Guilford Press, 46-76.
41. Keyes CLM, Myers JM, Kendler KS (2010): The structure of the genetic andenvironmental influencesonmental well-being.AmJ Public Health 100:2379-2384.
42. Keyes CLM (2002): The mental health continuum: from languishing to flourishing in life. J Health Soc Res 43:207-222.
43. Mroczek DK, Kolarz CM (1998): The effect of age on positive and negative affect: A developmental perspective on happiness. J Person Soc Psychol 75:1333-1349.
44. Keyes C (1998): Social well-being. Soc Psychol Q 61:121-140.
45. Spielberger C (1983): State-Trait Anxiety Inventory (Form Y).Palo Alto, CA: Consulting Psychologists Press.
46. Stohler C, Kowalski C (1999): Spatial and temporal summation of sensory and affective dimensions of deep somatic pain. Pain 79:165-173. (Pubitemid 29076751)
47. Zhang X, Ashton-Miller J, Stohler C, Anonymous (1993): A closed-loop system for maintaining constant experimental muscle pain in man. IEEE Trans Biomed Engineer 40:344-352.
48. Melzack R, Torgerson W (1971): On the language of pain. Anesthesiology 34:50-59.
49. Watson D, Clark LA, Tellegen A (1988): Development and validation of brief measures of positive and negative affect: The PANAS scales. J Person Soc Psychol 54:1063-1070.
50. Seeman P, Wilson A, Gmeiner P, Kapur S (2006): Dopamine D2 and D3 receptors in human putamen, caudate nucleus, and globus pallidus. Synapse 60:205-211. (Pubitemid 44036715)
51. Innis R, Malison R, al-Tikriti M, Hoffer P, Sybirska E, Seibyl J, et al. (1992): Amphetamine-stimulated dopamine release competes in vivo for [123I]IBZM binding to the D2 receptor in nonhuman primates. Synapse 10:177-184.
52. Meyer C, Boes J, Kim B, Bland P, Zasadny K, Kison P, et al. (1997): Demonstration of accuracy and clinical versatility of mutual information for automatic multimodality image fusion using affine and thinplate spline warped geometric deformations. Med Image Anal 1:195-206.
53. Munro CA, McCaul ME, Wong DF, Oswald LM, Zhou Y, Brasic J, et al. (2006): Sex differences in striatal dopamine release in healthy adults. Biol Psychiatry 59:966-974.
54. Riccardi P, Zald D, Li R, Park S, Ansari MS, Dawant B, et al. (2006): Sex differences in amphetamine-induced displacement of [(18)F]fallypride in striatal and extrastriatal regions: A PET study. Am J Psychiatry 163:1639-1641. (Pubitemid 44465768)
55. Brett M, Anton J-L, Valabregue R, Poline J-B (2002): Region of Interest Analysis Using an SPM Toolbox [abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain; June 2-6, 2002; Sendai, Japan. NeuroImage 16:497.
56. Rouge-Pont F, Piazza P, Kharouby M, Le Moal M, Simon H (1993): Higher and longer stress-induced increase in dopamine concentrations in the nucleus accumbens of animals predisposed to amphetamine self-administration. A microdialysis study. Brain Res 602:169-174. (Pubitemid 23045609)
57. Rouge-Pont F, Deroche V, Le Moal M, Piazza P (1998): Individual differences in stress-induced dopamine release in the nucleus accumbens are influenced by corticosterone. Eur J Neurosci 10:3903-3907. (Pubitemid 29073945)
58. Thierry A, Tassin J, Blanc G, Glowinski J (1976): Selective activation of mesocortical DA system by stress. Nature 263:242-244.
59. Pruessner JC, Champagne F, Meaney MJ, Dagher A (2004): Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: A positron emission tomography study using [11C]raclopride. J Neurosci 24:2825-2831. (Pubitemid 38380960)
60. Lataster J, Collip D, Ceccarini J, Haas D, Booij L, van Os J, et al. (2011): Psychosocial stress is associated with in vivo dopamine release in human ventromedial prefrontal cortex: A positron emission tomography study using [(18)F]fallypride. Neuroimage 58:1081-1089.
61. Cabib S, Puglisi-Allegra S, Ventura R (2002): The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behav Brain Res 130:103-109. (Pubitemid 34195327)
62. Stead JDH, Clinton S, Neal C, Schneider J, Jama A, Miller S, et al. (2006): Selective breeding for divergence in novelty-seeking traits: Heritability and enrichment in spontaneous anxiety-related behaviors. Behav Genet 36:697-712. (Pubitemid 44188085)
63. Erblich J, Lerman C, Self DW, Diaz GA, Bovbjerg DH (2004): Stress-induced cigarette craving: Effects of the DRD2 TaqI RFLP and SLC6A3 VNTR polymorphisms. Pharmacogenom J 4:102-109. (Pubitemid 38499993)
64. Brody AL, Mandelkern MA, Olmstead RE, Scheibal D, Hahn E, Shiraga S, et al. (2006): Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. Arch Gen Psychiatry 63:808-816.
65. Wood PB, Schweinhardt P, Jaeger E, Dagher A, Hakyemez H, Rabiner EA, et al. (2007): Fibromyalgia patients show an abnormal dopamine response to pain. Eur J Neurosci 25:3576-3582. (Pubitemid 47020461)
66. Haber SN, Knutson B (2009): The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology 35:4-26.
67. Kalivas PW, Nakamura M (1999): Neural systems for behavioral activation and reward. Curr Opin Neurobiol 9:223-227. (Pubitemid 29201796)
68. Mogenson G, Yang C (1991): The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv Exp Med Biol 295:267-290.
69. Lundeberg T, Uvnäs-Moberg K, Agren G, Bruzelius G (1994): Anti-nociceptive effects of oxytocin in rats and mice. Neurosci Letters 170:153-157. (Pubitemid 24117310)
70. Ge Y, Lundeberg T, Yu L-C (2002): Blockade effect of mu and kappa opioid antagonists on the anti-nociception induced by intra-periaqueductal grey injection of oxytocin in rats. Brain Res 927:204-207. (Pubitemid 34124127)
71. Gao L, Yu L-C (2004): Involvement of opioid receptors in the oxytocin-induced antinociception in the central nervous system of rats. Regul Pept 120:53-58. (Pubitemid 38726191)
72. de Oliveira DCG, Zuardi AW, Graeff FG, Queiroz RHC, Crippa JAS (2011): Anxiolytic-like effect of oxytocin in the simulated public speaking test [published online ahead of print May 9]. J Psychopharmacology.
73. Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U (2003): Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 54:1389-1398. (Pubitemid 37522163)
74. Ring RH, Malberg JE, Potestio L, Ping J, Boikess S, Luo B, et al. (2006): Anxiolytic-like activity of oxytocin in male mice: Behavioral and autonomic evidence, therapeutic implications. Psychopharmacology 185: 218-225. (Pubitemid 43363618)
75. Uvnäs-Moberg K (1998): Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrinology 23:819-835.
76. Schorscher-Petcu A, Sotocinal S, Ciura S, Dupré A, Ritchie J, Sorge RE, et al. (2010): Oxytocin-induced analgesia and scratching are mediated by the vasopressin-1A receptor in the mouse. J Neurosci 30:8274-8284.
77. Jacob S, Brune CW, Carter CS, Leventhal BL, Lord C, Cook EH (2007): Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism. Neurosci Lett 417:6-9. (Pubitemid 46517832)
78. Lerer E, Levi S, Salomon S, Darvasi A, Yirmiya N, Ebstein RP (2008): Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition. Mol Psychiatry 13:980-988.
79. Wermter A, Kamp-Becker I, Hesse P, Schulte-Körne G, Strauch K, Remschmidt H (2009): Evidence for the involvement of genetic variation in the oxytocin receptor gene (OXTR) in the etiology of autistic disorders on high-functioning level. Am J Med Genet Part B 153B:629-639.
80. Wu S, Jia M, Ruan Y, Liu J, Guo Y, Shuang M, et al. (2005): Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biol Psychiatry 58:74-77. (Pubitemid 40909939)
81. Costa B, Pini S, Gabelloni P, Abelli M, Lari L, Cardini A, et al. (2009): Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology 34:1506-1514.
82. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011): Oxytocin and vasopressin in the human brain: Social neuropeptides for translational medicine. Nature Rev Neurosci 12:524-538.
83. Carter CS (2007): Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders? Behav Brain Res 176:170-186.
84. Gimpl G, Fahrenholz F (2001): The oxytocin receptor system: Structure, function, and regulation. Physiol Rev 81:629-683. (Pubitemid 32267075)
85. Insel TR, Shapiro LE (1992): Oxytocin receptors and maternal behavior. Ann N Y Acad Sci 652:122-141.
86. Nomura M, McKenna E, Korach KS, Pfaff DW, Ogawa S (2002): Estrogen receptor-beta regulates transcript levels for oxytocin and arginine va- sopressin in the hypothalamic paraventricular nucleus of male mice. Mol Brain Res 109:84-94. (Pubitemid 36078376)
87. Witt DM, Carter CS, Lnsel TR (1991): Oxytocin receptor binding in female prairie voles: Endogenous and exogenous oestradiol stimulation. J Neuroendocrinol 3:155-161.
88. Andersson KE (2001): Pharmacology of penile erection. Pharmacol Rev 53:417-450.
89. Bales KL, Pfeifer LA, Carter CS (2004): Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles. Dev Psychobiol 44:123-131. (Pubitemid 38270594)
90. Wang ZX, Liu Y, Young LJ, Insel TR (2000): Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent. J Neuroendocrinol 12:111-120. (Pubitemid 30098892)
91. Gabor CS, Phan A, Clipperton-Allen AE, Kavaliers M, Choleris E (2012): Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav Neuroscience 126:97-109.
92. Barraza JA, Zak PJ (2009): Empathy toward strangers triggers oxytocin release and subsequent generosity. Ann N Y Acad Sci 1167:182-189.
93. Domes G, Heinrichs M, Gläscher J, Büchel C, Braus DF, Herpertz SC (2007): Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62:1187-1190. (Pubitemid 350029722)
94. Kirsch P, Esslinger C, Chen Q, Mier D, Lis S, Siddhanti S, et al. (2005): Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 25:11489-11493. (Pubitemid 43083720)
95. Domes G, Lischke A, Berger C, Grossmann A, Hauenstein K, Heinrichs M, et al. (2010): Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35:83-93.
96. Tost H, Kolachana B, Hakimi S, Lemaitre H, Verchinski BA, Mattay VS, et al. (2010): A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc Natl Acad Sci U S A 107:13936-13941.
97. Southwick SM, Vythilingam M, Charney DS (2005): The psychobiology of depression and resilience to stress: Implications for prevention and treatment. Annu Rev Clin Psychol 1:255-291. (Pubitemid 43843952)
98. Lodge DJ, Grace AA (2011): Developmental pathology, dopamine, stress and schizophrenia. Int J Dev Neurosci 29:207-213.
99. Ungless MA, Argilli E, Bonci A (2010): Effects of stress and aversion on dopamine neurons: Implications for addiction. Neurosci Biobehav Rev 35:151-156.
100. Becker JB, Hu M (2008): Sex differences in drug abuse. Front Neuroendocrinol 29:36-47.