Oxytocin enhances attractiveness of unfamiliar female faces independent of the dopamine reward system

Psychoneuroendocrinology

Volumn 39, Issue 1, 2014, Pages 74-87

  Striepens, Nadine ^a   Matusch, Andreas ^b   Kendrick, Keith M ^d   Mihov, Yoan ^a   Elmenhorst, David ^b   Becker, Benjamin ^a   Lang, Markus ^b   Coenen, Heinz H ^b   Maier, Wolfgang ^a,c   Hurlemann, René ^a   Bauer, Andreas ^b,e  

^a UNIVERSITY OF BONN   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

^e HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Attractiveness; Dopamine; Face; Familiarity; Oxytocin; PET; Raclopride; Reward; Striatum

Indexed keywords

DOPAMINE; DOPAMINE 2 RECEPTOR; OXYTOCIN; RACLOPRIDE C 11;

ADULT; ARTICLE; BRAIN FUNCTION; BRAIN PERFUSION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DRUG PROTEIN BINDING; FACE; FAMILIARITY; GLOBUS PALLIDUS; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; OXYTOCIN BLOOD LEVEL; PERCEPTION; PHYSICAL ATTRACTIVENESS; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REWARD; SUPERIOR PARIETAL LOBULE; TASK PERFORMANCE; AMYGDALOID NUCLEUS; CINGULUM (BRAIN); DOPAMINERGIC SYSTEM; FACE PROFILE; FEMALE; INFERIOR FRONTAL GYRUS; INSULA; MIDDLE FRONTAL GYRUS; OCCIPITAL CORTEX; ORBITAL CORTEX; PARIETAL CORTEX; PARIETAL GYRUS; PROTEIN BINDING; SUPERIOR FRONTAL GYRUS; TEMPORAL CORTEX; THALAMUS;

ATTRACTIVENESS; DOPAMINE; FACE; FAMILIARITY; MAGNETIC RESONANCE IMAGING; MNI; MONTREAL NEUROLOGICAL INSTITUTE; MRI; OXYTOCIN; PET; POSITRON EMISSION TOMOGRAPHY; RACLOPRIDE; REWARD; STRIATUM;

ADULT; CORPUS STRIATUM; DOPAMINE; DOUBLE-BLIND METHOD; FACE; FEMALE; HUMANS; MALE; OXYTOCIN; RACLOPRIDE;

EID: 84888057308     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2013.09.026     Document Type: Article

References (64)

1. Aharon I., Etcoff N., Ariely D., Chabris C.F., O'Connor E., Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 2001, 32:537-551.
2. Bartels A., Zeki S. The neural basis of romantic love. Neuroreport 2000, 11:3829-3834.
3. Bartels A., Zeki S. The neural correlates of maternal and romantic love. Neuroimage 2004, 21:1155-1166.
4. Bartz J.A., Zaki J., Bolger N., Ochsner K.N. Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 2011, 15:301-309.
5. Baumgartner T., Heinrichs M., Vonlanthen A., Fischbacher U., Fehr E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 2008, 58:639-650.
6. Born J., Lange T., Kern W., McGregor G.P., Bickel U., Fehm H.L. Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 2002, 5:514-516.
7. Bray S., O'Doherty J. Neural coding of reward-prediction error signals during classical conditioning with attractive faces. J. Neurophysiol. 2007, 97:3036-3045.
8. Bethlehem R.A.I., van Honk J., Auyeung B., Baron-Cohen S. Oxytocin, brain physiology, and functional connectivity: a review of intranasal oxytocin fMRI studies. Psychoneuroendocrinology 2013, 38:962-974.
9. Burkett J.P., Spiegel L.L., Inoue K., Murphy A.Z., Young L.J. Activation of μ-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles. Neuropsychopharmacology 2011, 36:2200-2210.
10. Cloutier J., Heatherton T.F., Whalen P.J., Kelley W.M. Are attractive people rewarding? Sex differences in the neural substrates of facial attractiveness. J. Cogn. Neurosci. 2008, 20:941-951.
11. De Dreu C.K., Greer L.L., Handgraaf M.J., Shalvi S., Van Kleef G.A., Baas M., Ten Velden F.S., Van Dijk E., Feith S.W. The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 2010, 328:1408-1411.
12. Dölen G., Darvishzadeh A., Huang K.W., Malenka R.C. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013, 501:179-184.
13. Domes G., Heinrichs M., Michel A., Berger C., Herpertz S.C. Oxytocin improves mind-reading in humans. Biol. Psychiatry 2007, 61:731-733.
14. Domes G., Lischke A., Berger C., Grossmann A., Hauenstein K., Heinrichs M., Herpertz S.C. Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 2010, 35:83-93.
15. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
16. Fusar-Poli P., Placentino A., Carletti F., Landi P., Allen P., Surguladze S., Benedetti F., Abbamonte M., Gasparotti R., Barale F., Perez J., McGuire P., Politi P. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J. Psychiatry Neurosci. 2009, 34:418-432.
17. Gamer M., Zurowski B., Buchel C. Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc. Natl. Acad. Sci. USA 2010, 107:9400-9405.
18. Garraux G., Peigneux P., Carson R.E., Hallett M. Task-related interaction between basal ganglia and cortical dopamine release. J. Neurosci. 2007, 27:14434-14441.
19. Goldin P.R., McRae K., Ramel W., Gross J.J. The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biol. Psychiatry 2008, 63:577-586.
20. Greene J., Haidt J. How (and where) does moral judgment work?. Trends Cogn. Sci. 2002, 6:517-523.
21. Gregory K.J., Sexton P.M., Christopoulos A. Overview of receptor allosterism. Curr. Protoc. Pharmacol. 2010, (Chapter 1, Unit 1 21).
22. Grillon C., Krimsky M., Charney D.R., Vytal K., Ernst M., Cornwell B. Oxytocin increases anxiety to unpredictable threat. Mol. Psychiatry 2012, 18:958-960.
23. Grunder G., Landvogt C., Vernaleken I., Buchholz H.G., Ondracek J., Siessmeier T., Hartter S., Schreckenberger M., Stoeter P., Hiemke C., Rosch F., Wong D.F., Bartenstein P. The striatal and extrastriatal D2/D3 receptor-binding profile of clozapine in patients with schizophrenia. Neuropsychopharmacology 2006, 31:1027-1035.
24. Hirvonen J., Aalto S., Lumme V., Nagren K., Kajander J., Vilkman H., Hagelberg N., Oikonen V., Hietala J. Measurement of striatal and thalamic dopamine D2 receptor binding with 11C-raclopride. Nucl. Med. Commun. 2003, 24:1207-1214.
25. Hurlemann R., Patin A., Onur O.A., Cohen M.X., Baumgartner T., Metzler S., Dziobek I., Gallinat J., Wagner M., Maier W., Kendrick K.M. Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J. Neurosci. 2010, 30:4999-5007.
26. Insel T.R., Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. USA 1992, 89:5981-5985.
27. Katanoda K., Yoshikawa K., Sugishita M. Neural substrates for the recognition of newly learned faces: a functional MRI study. Neuropsychologia 2000, 38:1616-1625.
28. Kendrick K.M. Oxytocin, motherhood and bonding. Exp. Physiol. 2000, 85:111S-124S.
29. Kendrick K.M., Keverne E.B., Baldwin B.A. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 1987, 46:56-61.
30. Kessler R.M., Ansari M.S., Riccardi P., Li R., Jayathilake K., Dawant B., Meltzer H.Y. Occupancy of striatal and extrastriatal dopamine D2/D3 receptors by olanzapine and haloperidol. Neuropsychopharmacology 2005, 30:2283-2289.
31. Koepp M.J., Gunn R.N., Lawrence A.D., Cunningham V.J., Dagher A., Jones T., Brooks D.J., Bench C.J., Grasby P.M. Evidence for striatal dopamine release during a video game. Nature 1998, 393:266-268.
32. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
33. Lammertsma A.A., Hume S.P. Simplified reference tissue model for PET receptor studies. Neuroimage 1996, 4:153-158.
34. Laruelle M. Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J. Cereb. Blood Flow Metab. 2000, 20:423-451.
35. Liang X., Zebrowitz L.A., Zhang Y. Neural activation in the reward circuit shows a nonlinear response to facial attractiveness. Soc. Neurosci. 2010, 5:320-334.
36. Lim M.M., Murphy A.Z., Young L.J. Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster). J. Comp. Neurol. 2004, 468:555-570.
37. Liu Y., Wang Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 2003, 121:537-544.
38. 11C]raclopride binding in the brain: model simulations and kinetic analysis of PET data. J. Cereb. Blood Flow Metab. 1994, 14:995-1010.
39. Loup F., Tribollet E., Dubois-Dauphin M., Dreifuss J.J. Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res. 1991, 555:220-232.
40. Love T.M., Enoch M.A., Hodgkinson C.A., Peciña M., Mickey B., Koeppe R.A., Stohler C.S., Goldman D., Zubieta J.K. Oxytocin gene polymorphisms influence human dopaminergic function in a sex-dependent manner. Biol. Psychiatry 2012, 72:198-206.
41. MacDonald E., Dadds M.R., Brennan J.L., Williams K., Levy F., Cauchi A.J. A review of safety, side-effects and subjective reactions to intranasal oxytocin in human research. Psychoneuroendocrinology 2011, 36:1114-1126.
42. Mukherjee J., Yang Z.Y., Das M.K., Brown T. Fluorinated benzamide neuroleptics - III. Development of (S)-N-[(1-allyl-2-pyrrolidinyl)methyl]-5-(3-[18F]fluoropropyl)-2, 3-dimethoxybenzamide as an improved dopamine D-2 receptor tracer. Nucl. Med. Biol. 1995, 22:283-296.
43. Neumann I.D., Maloumby R., Beiderbeck D.I., Likas M., Landgraf R. Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology 2013, 38:1985-1993.
44. Rilling J.K., DeMarco A.C., Hackett P.D., Thompson R., Ditzen B., Patel R., Pagnoni G. Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology 2012, 37:447-461.
45. Romero-Fernandez W., Borroto-Escuela D.O., Agnati L.F., Fuxe K. Evidence for the existence of dopamine d2-oxytocin receptor heteromers in the ventral and dorsal striatum with facilitatory receptor-receptor interactions. Mol. Psychiatry 2012, 18:849-850.
46. Sawamoto N., Piccini P., Hotton G., Pavese N., Thielemans K., Brooks D.J. Cognitive deficits and striato-frontal dopamine release in Parkinson's disease. Brain: J. Neurol. 2008, 131:1294-1302.
47. Scheele D., Striepens N., Gunturkun O., Deutschlander S., Maier W., Kendrick K.M., Hurlemann R. Oxytocin modulates social distance between males and females. J. Neurosci. 2012, 32:16074-16079.
48. Scheele, D., Wille, A., Kendrick, K., Becker, B., Gunturkun, O., Maier, W., Hurlemann, R., 2013. Intranasal oxytocin interacts with dopaminergic brain reward areas to strengthen romantic bonds, submitted for publication.
49. Schott B.H., Minuzzi L., Krebs R.M., Elmenhorst D., Lang M., Winz O.H., Seidenbecher C.I., Coenen H.H., Heinze H.J., Zilles K., Duzel E., Bauer A. Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J. Neurosci. 2008, 28:14311-14319.
50. Skuse D.H., Gallagher L. Dopaminergic-neuropeptide interactions in the social brain. Trends Cogn. Sci. 2009, 13:27-35.
51. 11C]-raclopride binding after THC challenge. Neuroimage 2010, 52:1521-1527.
52. Striepens N., Kendrick K.M., Maier W., Hurlemann R. Prosocial effects of oxytocin and clinical evidence for its therapeutic potential. Front. Neuroendocrinol. 2011, 32:426-450.
53. Striepens N., Scheele D., Kendrick K.M., Becker B., Schafer L., Schwalba K., Reul J., Maier W., Hurlemann R. Oxytocin facilitates protective responses to aversive social stimuli in males. Proc. Natl. Acad. Sci. USA 2012, 109:18144-18149.
54. Theodoridou A., Rowe A.C., Penton-Voak I.S., Rogers P.J. Oxytocin and social perception: oxytocin increases perceived facial trustworthiness and attractiveness. Horm. Behav. 2009, 56:128-132.
55. Todorov A. The role of the amygdala in face perception and evaluation. Motiv. Emot. 2012, 36:16-26.
56. Todorov A., Said C.P., Oosterhof N.N., Engell A.D. Task-invariant brain responses to the social value of faces. J. Cogn. Neurosci. 2011, 23:2766-2781.
57. Tsukada H., Nishiyama S., Kakiuchi T., Ohba H., Sato K., Harada N. Is synaptic dopamine concentration the exclusive factor which alters the in vivo binding of [11C]raclopride?: PET studies combined with microdialysis in conscious monkeys. Brain Res. 1999, 841:160-169.
58. Tsukiura T., Cabeza R. Remembering beauty: roles of orbitofrontal and hippocampal regions in successful memory encoding of attractive faces. Neuroimage 2011, 54:653-660.
59. Wang G.J., Volkow N.D., Fowler J.S., Logan J., Pappas N.R., Wong C.T., Hitzemann R.J., Netusil N. Reproducibility of repeated measures of endogenous dopamine competition with [11C]raclopride in the human brain in response to methylphenidate. J. Nucl. Med. 1999, 40:1285-1291.
60. Williams J.R., Insel T.R., Harbaugh C.R., Carter C.S. Oxytocin administered centrally facilitates formation of a partner preference in female Prairie voles (microtus ochrogaster). J. Neuroendocrinol. 1994, 6:247-250.
61. Winston J.S., O'Doherty J., Kilner J.M., Perrett D.I., Dolan R.J. Brain systems for assessing facial attractiveness. Neuropsychologia 2007, 45:195-206.
62. Yamasue H., Yee J.R., Hurlemann R., Rilling J.K., Chen F.S., Meyer-Lindenberg A., Tost H. Integrative approaches utilizing oxytocin to enhance prosocial behavior: from animal and human social behavior to autistic social dysfunction. J. Neurosci. 2012, 32:14109-14117.
63. 11C]raclopride-binding potential in nontreatment-seeking alcoholics. Synapse 2011, 65:553-561.
64. Zeki S. The neurobiology of love. FEBS Lett. 2007, 581:2575-2579.