Intranasal oxytocin effects on social cognition: A critique

Brain Research

Volumn 1580, Issue , 2014, Pages 69-77

  Evans, Simon L ^a   Dal Monte, Olga ^b,c   Noble, Pamela ^b   Averbeck, Bruno B ^b  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Anxiety; CSF; Intranasal administration; Oxytocin; Pro social neuropeptide; Social cognition; Social stimuli

Indexed keywords

NOSE SPRAY; OXYTOCIN; OXYTOCIN RECEPTOR; PSYCHOTROPIC AGENT;

ARTICLE; AUTISM; BEHAVIOR CHANGE; CENTRAL NERVOUS SYSTEM; DRUG BLOOD LEVEL; DRUG CEREBROSPINAL FLUID LEVEL; DRUG DELIVERY SYSTEM; DRUG DIFFUSION; DRUG EFFECT; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG RELEASE; FACIAL EXPRESSION; HUMAN; HUMAN RELATION; MEMORY; NONHUMAN; RANDOMIZED CONTROLLED TRIAL (TOPIC); SCHIZOPHRENIA; SOCIAL BEHAVIOR; SOCIAL COGNITION; SYSTEMATIC REVIEW (TOPIC); TRANQUILIZING ACTIVITY; TRUST; ANIMAL; COGNITION; DRUG EFFECTS; INTRANASAL DRUG ADMINISTRATION; PHYSIOLOGY;

ADMINISTRATION, INTRANASAL; ANIMALS; COGNITION; HUMANS; OXYTOCIN; PSYCHOTROPIC DRUGS; SOCIAL BEHAVIOR;

EID: 84907709374     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.11.008     Document Type: Article

References (104)

1. R. Adolphs, D. Tranel, and A.R. Damasio The human amygdala in social judgment Nature 393 1998 470 474
2. J.A. Amico, S.M. Challinor, and J.L. Cameron Pattern of oxytocin concentrations in the plasma and cerebrospinal fluid of lactating rhesus monkeys (Macaca mulatta): evidence for functionally independent oxytocinergic pathways in primates J. Clin. Endocrinol. Metab. 71 1990 1531 1535
3. E. Andari, J.R. Duhamel, T. Zalla, E. Herbrecht, M. Leboyer, and A. Sirigu Promoting social behavior with oxytocin in high-functioning autism spectrum disorders Proc. Natl. Acad. Sci. U. S. A. 107 2010 4389 4394
4. K.L. Bales, A.M. Perkeybile, O.G. Conley, M.H. Lee, C.D. Guoynes, G.M. Downing, C.R. Yun, M. Solomon, S. Jacob, and S.P. Mendoza Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles Biol. Psychiatry 74 2013 180 188
5. J.A. Bartz, J. Zaki, N. Bolger, E. Hollander, N.N. Ludwig, A. Kolevzon, and K.N. Ochsner Oxytocin selectively improves empathic accuracy Psychol. Sci. 21 2010 1426 1428
6. J.A. Bartz, J. Zaki, N. Bolger, and K.N. Ochsner Social effects of oxytocin in humans: context and person matter Trends Cogn. Sci. 15 2011 301 309
7. T. Baumgartner, M. Heinrichs, A. Vonlanthen, U. Fischbacher, and E. Fehr Oxytocin shapes the neural circuitry of trust and trust adaptation in humans Neuron 58 2008 639 650
8. J. Born, T. Lange, W. Kern, G.P. McGregor, U. Bickel, and H.L. Fehm Sniffing neuropeptides: a transnasal approach to the human brain Nat. Neurosci. 5 2002 514 516
9. O.J. Bosch, S.L. Meddle, D.I. Beiderbeck, A.J. Douglas, and I.D. Neumann Brain oxytocin correlates with maternal aggression: link to anxiety J. Neurosci. 25 2005 6807 6815
10. A. Burri, M. Heinrichs, M. Schedlowski, and T.H. Kruger The acute effects of intranasal oxytocin administration on endocrine and sexual function in males Psychoneuroendocrinology 33 2008 591 600
11. D.S. Carson, A.J. Guastella, E.R. Taylor, and I.S. McGregor A brief history of oxytocin and its role in modulating psychostimulant effects J. Psychopharmacol. 27 2013 231 247
12. C.S. Carter, M. Altemus, and G.P. Chrousos Neuroendocrine and emotional changes in the post-partum period Prog. Brain Res. 133 2001 241 249
13. C.S. Carter Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav. Brain Res. 176 2007 170 186
14. S.M. Challinor, S.J. Winters, and J.A. Amico Pattern of oxytocin concentrations in the peripheral blood of healthy women and men: effect of the menstrual cycle and short-term fasting Endocr. Res. 20 1994 117 125
15. S.W. Chang, J.W. Barter, R.B. Ebitz, K.K. Watson, and M.L. Platt Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta) Proc. Natl. Acad. Sci. U. S. A. 109 2012 959 964
16. P.S. Churchland, and P. Winkielman Modulating social behavior with oxytocin: how does it work? What does it mean? Horm. Behav. 61 2012 392 399
17. G. Corona, E.A. Jannini, L. Vignozzi, G. Rastrelli, and M. Maggi The hormonal control of ejaculation Nat. Rev. Urol. 9 2012 508 519
18. F. Courtois, S. Carrier, K. Charvier, P.A. Guertin, and N.M. Journel The control of male sexual responses Curr. Pharm. Des. 19 2013 4341 4356
19. J.M. Cyranowski, T.L. Hofkens, E. Frank, H. Seltman, H.M. Cai, and J.A. Amico Evidence of dysregulated peripheral oxytocin release among depressed women Psychosom. Med. 70 2008 967 975
20. C.K. De Dreu, L.L. Greer, M.J. Handgraaf, S. Shalvi, G.A. Van Kleef, M. Baas, F.S. Ten Velden, E. Van Dijk, and S.W. Feith The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans Science 328 2010 1408 1411
21. D.C. de Oliveira, A.W. Zuardi, F.G. Graeff, R.H. Queiroz, and J.A. Crippa Anxiolytic-like effect of oxytocin in the simulated public speaking test J. Psychopharmacol. 26 2012 497 504
22. C.H. Declerck, C. Boone, and T. Kiyonari Oxytocin and cooperation under conditions of uncertainty: the modulating role of incentives and social information Horm. Behav. 57 2010 368 374
23. M. Di Simplicio, R. Massey-Chase, P.J. Cowen, and C.J. Harmer Oxytocin enhances processing of positive versus negative emotional information in healthy male volunteers J. Psychopharmacol. 23 2009 241 248
24. B. Ditzen, M. Schaer, B. Gabriel, G. Bodenmann, U. Ehlert, and M. Heinrichs Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict Biol. Psychiatry 65 2009 728 731
25. G. Domes, M. Heinrichs, J. Glascher, C. Buchel, D.F. Braus, and S.C. Herpertz Oxytocin attenuates amygdala responses to emotional faces regardless of valence Biol. Psychiatry 62 2007 1187 1190
26. G. Domes, A. Lischke, C. Berger, A. Grossmann, K. Hauenstein, M. Heinrichs, and S.C. Herpertz Effects of intranasal oxytocin on emotional face processing in women Psychoneuroendocrinology 35 2010 83 93
27. G. Domes, M. Sibold, L. Schulze, A. Lischke, S.C. Herpertz, and M. Heinrichs Intranasal oxytocin increases covert attention to positive social cues Psychol. Med. 43 2013 1747 1753
28. S. Evans, S.S. Shergill, and B.B. Averbeck Oxytocin decreases aversion to angry faces in an associative learning task Neuropsychopharmacology 35 2010 2502 2509
29. N. Falke Oxytocin stimulates oxytocin release from isolated nerve terminals of rat neural lobes Neuropeptides 14 1989 269 274
30. J.N. Ferguson, J.M. Aldag, T.R. Insel, and L.J. Young Oxytocin in the medial amygdala is essential for social recognition in the mouse J. Neurosci. 21 2001 8278 8285
31. J.N. Ferguson, L.J. Young, and T.R. Insel The neuroendocrine basis of social recognition Front Neuroendocrinol. 23 2002 200 224
32. M. Fischer-Shofty, S.G. Shamay-Tsoory, H. Harari, and Y. Levkovitz The effect of intranasal administration of oxytocin on fear recognition Neuropsychologia 48 2010 179 184
33. M. Gamer, B. Zurowski, and C. Buchel Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans Proc. Natl. Acad. Sci. U. S. A. 107 2010 9400 9405
34. G. Gimple, and F. Farenholtz The oxytocin receptor system: structure, function, and regulation Physiol. Rev. 81 2001 629 683
35. M. Goldman, M. Marlow-O'Connor, I. Torres, and C.S. Carter Diminished plasma oxytocin in schizophrenic patients with neuroendocrine dysfunction and emotional deficits Schizophr. Res. 98 2008 247 255
36. M.B. Goldman, A.M. Gomes, C.S. Carter, and R. Lee Divergent effects of two different doses of intranasal oxytocin on facial affect discrimination in schizophrenic patients with and without polydipsia Psychopharmacology (Berl). 216 2011 101 110
37. A. Gossen, A. Hahn, L. Westphal, S. Prinz, R.T. Schultz, G. Grunder, and K.N. Spreckelmeyer Oxytocin plasma concentrations after single intranasal oxytocin administration-A study in healthy men Neuropeptides 46 2012 211 215
38. L. Green, D. Fein, C. Modahl, C. Feinstein, L. Waterhouse, and M. Morris Oxytocin and autistic disorder: alterations in peptide forms Biol. Psychiatry 50 2001 609 613
39. K.M. Grewen, S.S. Girdler, J. Amico, and K.C. Light Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact Psychosom. Med. 67 2005 531 538
40. A.J. Grippo, D. Gerena, J. Huang, N. Kumar, M. Shah, R. Ughreja, and C.S. Carter Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles Psychoneuroendocrinology 32 2007 966 980
41. A.J. Guastella, P.B. Mitchell, and M.R. Dadds Oxytocin increases gaze to the eye region of human faces Biol. Psychiatry 63 2008 3 5
42. A.J. Guastella, P.B. Mitchell, and F. Mathews Oxytocin enhances the encoding of positive social memories in humans Biol. Psychiatry 64 2008 256 258
43. A.J. Guastella, S.L. Einfeld, K.M. Gray, N.J. Rinehart, B.J. Tonge, T.J. Lambert, and I.B. Hickie Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders Biol. Psychiatry 67 2010 692 694
44. A.J. Guastella, I.B. Hickie, M.M. McGuinness, M. Otis, E.A. Woods, H.M. Disinger, H.K. Chan, T.F. Chen, and R.B. Banati Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research Psychoneuroendocrinology 38 2013 612 625
45. J.V. Haxby, E.A. Hoffman, and M.I. Gobbini The distributed human neural system for face perception Trends Cogn. Sci. 4 2000 223 233
46. C. Heim, L.J. Young, D.J. Newport, T. Mletzko, A.H. Miller, and C.B. Nemeroff Lower CSF oxytocin concentrations in women with a history of childhood abuse Mol. Psychiatry 14 2009 954 958
47. M. Heinrichs, G. Meinlschmidt, I. Neumann, S. Wagner, C. Kirschbaum, U. Ehlert, and D.H. Hellhammer Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women J. Clin. Endocrinol. Metab. 86 2001 4798 7804
48. M. Heinrichs, T. Baumgartner, C. Kirschbaum, and U. Ehlert Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress Biol. Psychiatry 54 2003 1389 1398
49. E. Hollander, S. Novotny, M. Hanratty, R. Yaffe, C.M. DeCaria, B.R. Aronowitz, and S. Mosovich Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders Neuropsychopharmacology 28 2003 193 198
50. R. Hurlemann, A. Patin, O.A. Onur, M.X. Cohen, T. Baumgartner, S. Metzler, I. Dziobek, J. Gallinat, M. Wagner, W. Maier, and K.M. Kendrick Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans J. Neurosci. 30 2010 4999 5007
51. T.R. Insel, and L.E. Shapiro Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles Natl. Acad. Sci. U. S. A. 89 1992 5981 5985
52. T.R. Insel, and R.D. Fernald How the brain processes social information: searching for the social brain Annu. Rev. Neurosci. 27 2004 697 722
53. I.A. Ionescu, J. Dine, Y.C. Yen, D.R. Buell, L. Herrmann, F. Holsboer, M. Eder, R. Landgraf, and U. Schmidt Intranasally administered neuropeptide S (NPS) exerts anxiolytic effects following internalization into NPS receptor-expressing neurons Neuropsychopharmacology 37 2012 1323 1337
54. P.M. Jones, and I.C. Robinson Differential clearance of neurophysin and neurohypophysial peptides from the cerebrospinal fluid in conscious guinea pigs Neuroendocrinology 34 1982 297 302
55. R. Kawashima, M. Sugiura, T. Kato, A. Nakamura, K. Hatano, K. Ito, H. Fukuda, S. Kojima, and K. Nakamura The human amygdala plays an important role in gaze monitoring. A PET study Brain 122 Pt 4 1999 779 783
56. S. Keri, I. Kiss, and O. Kelemen Sharing secrets: oxytocin and trust in schizophrenia Soc. Neurosci. 4 2009 287 293
57. M. Kosfeld, M. Heinrichs, P.J. Zak, U. Fischbacher, and E. Fehr Oxytocin increases trust in humans Nature 435 2005 673 676
58. L.D. Kubzansky, W.B. Mendes, A.A. Appleton, J. Block, and G.K. Adler A heartfelt response: oxytocin effects on response to social stress in men and women Biol. Psychol. 90 2012 1 9
59. K.C. Light, K.M. Grewen, and J.A. Amico More frequent partner hugs and higher oxytocin levels are linked to lower blood pressure and heart rate in premenopausal women Biol. Psychol. 69 2005 5 21
60. A. Lischke, C. Berger, K. Prehn, M. Heinrichs, S.C. Herpertz, and G. Domes Intranasal oxytocin enhances emotion recognition from dynamic facial expressions and leaves eye-gaze unaffected Psychoneuroendocrinology 37 2012 475 481
61. A. Lischke, M. Gamer, C. Berger, A. Grossmann, K. Hauenstein, M. Heinrichs, S.C. Herpertz, and G. Domes Oxytocin increases amygdala reactivity to threatening scenes in females Psychoneuroendocrinology 37 2012 1431 1438
62. E. MacDonald, M.R. Dadds, J.L. Brennan, K. Williams, F. Levy, and A.J. Cauchi A review of safety, side-effects and subjective reactions to intranasal oxytocin in human research Psychoneuroendocrinology 36 2011 1114 1126
63. R.C. Mantella, R.R. Vollmer, X. Li, and J.A. Amico Female oxytocin-deficient mice display enhanced anxiety-related behavior Endocrinology 144 2003 2291 2296
64. A.A. Marsh, H.H. Yu, D.S. Pine, and R.J. Blair Oxytocin improves specific recognition of positive facial expressions Psychopharmacology (Berl). 209 2010 225 232
65. M.M. McCarthy, C.H. McDonald, P.J. Brooks, and D. Goldman An anxiolytic action of oxytocin is enhanced by estrogen in the mouse Physiol. Behav. 60 1996 1209 1215
66. B.B. McEwen Brain-fluid barriers: relevance for theoretical controversies regarding vasopressin and oxytocin memory research Adv. Pharmacol. 50 2004 655 708
67. W.B. Mens, F. Laczi, J.A. Tonnaer, E.R. de Kloet, and T.B. van Wimersma Greidanus Vasopressin and oxytocin content in cerebrospinal fluid and in various brain areas after administration of histamine and pentylenetetrazol Pharmacol. Biochem. Behav. 19 1983 587 591
68. M. Mikolajczak, N. Pinon, A. Lane, P. de Timary, and O. Luminet Oxytocin not only increases trust when money is at stake, but also when confidential information is in the balance Biol. Psychol. 85 2010 182 184
69. C. Modahl, L. Green, D. Fein, M. Morris, L. Waterhouse, C. Feinstein, and H. Levin Plasma oxytocin levels in autistic children Biol. Psychiatry 43 1998 270 277
70. F. Moos, M.J. Freund-Mercier, Y. Guerne, J.M. Guerne, M.E. Stoeckel, and P. Richard Release of oxytocin and vasopressin by magnocellular nuclei in vitro: specific facilitatory effect of oxytocin on its own release J. Endocrinol. 102 1984 63 72
71. I.D. Neumann, R. Maloumby, D.I. Beiderbeck, M. Lukas, and R. Landgraf Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice Psychoneuroendocrinology 38 2013 1985 1993
72. N. Nonaka, S.A. Farr, H. Kageyama, S. Shioda, and W.A. Banks Delivery of galanin-like peptide to the brain: targeting with intranasal delivery and cyclodextrins J. Pharmacol. Exp. Ther. 325 2008 513 519
73. K.J. Parker, C.L. Hoffman, S.A. Hyde, C.S. Cummings, and D. Maestripieri Effects of age on cerebrospinal fluid oxytocin levels in free-ranging adult female and infant rhesus macaques Behav. Neurosci. 124 2010 428 433
74. C.A. Pedersen, and A.J. Prange Jr. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin Proc. Natl. Acad. Sci. U. S. A. 76 1979 6661 6665
75. K. Prehn, P. Kazzer, A. Lischke, M. Heinrichs, S.C. Herpertz, and G. Domes Effects of intranasal oxytocin on pupil dilation indicate increased salience of socioaffective stimuli Psychophysiology 50 2013 528 537
76. U. Rimmele, K. Hediger, M. Heinrichs, and P. Klaver Oxytocin makes a face in memory familiar J. Neurosci. 29 2009 38 42
77. R.H. Ring, J.E. Malberg, L. Potestio, J. Ping, S. Boikess, B. Luo, L.E. Schechter, S. Rizzo, Z. Rahman, and S. Rosenzweig-Lipson Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications Psychopharmacology (Berl). 185 2006 218 225
78. I.C. Robinson, R.G. Clark, K.M. Fairhall, P.M. Jones, and J.A. Parsons Effects of anti-oxytocin serum in Brattleboro rats Ann. N. Y. Acad. Sci. 394 1982 285 290
79. I.C. Robinson, and J.E. Coombes Neurohypophysial peptides in cerebrospinal fluid: an update Ann. N. Y. Acad. Sci. 689 1993 269 284
80. L.A. Rosenblum, E.L. Smith, M. Altemus, B.A. Scharf, M.J. Owens, C.B. Nemeroff, J.M. Gorman, and J.D. Coplan Differing concentrations of corticotropin-releasing factor and oxytocin in the cerebrospinal fluid of bonnet and pigtail macaques Psychoneuroendocrinology 27 2002 651 660
81. H.E. Ross, and L.J. Young Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior Front Neuroendocrinol. 30 2009 534 547
82. E. Savaskan, R. Ehrhardt, A. Schulz, M. Walter, and H. Schachinger Post-learning intranasal oxytocin modulates human memory for facial identity Psychoneuroendocrinology 33 2008 368 374
83. G. Scantamburlo, M. Hansenne, S. Fuchs, W. Pitchot, P. Marechal, C. Pequeux, M. Ansseau, and J.J. Legros Plasma oxytocin levels and anxiety in patients with major depression Psychoneuroendocrinology 32 2007 407 410
84. D. Scheele, N. Striepens, O. Gunturkun, S. Deutschlander, W. Maier, K.M. Kendrick, and R. Hurlemann Oxytocin modulates social distance between males and females J. Neurosci. 32 2012 16074 16079
85. I. Schneiderman, O. Zagoory-Sharon, J.F. Leckman, and R. Feldman Oxytocin during the initial stages of romantic attachment: relations to couples' interactive reciprocity Psychoneuroendocrinology 37 2012 1277 1285
86. J.R. Seckl, and S.L. Lightman Diurnal rhythm of vasopressin but not of oxytocin in the cerebrospinal fluid of the goat: lack of association with plasma cortisol rhythm J. Endocrinol. 114 1987 477 482
87. S.G. Shamay-Tsoory, M. Fischer, J. Dvash, H. Harari, N. Perach-Bloom, and Y. Levkovitz Intranasal Administration of Oxytocin Increases Envy and Schadenfreude (Gloating) Biol. Psychiatry 66 2009 864 870
88. T. Singer, R. Snozzi, G. Bird, P. Petrovic, G. Silani, M. Heinrichs, and R.J. Dolan Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain Emotion 8 2008 781 791
89. A.L. Smith, S.M. Freeman, J.S. Stehouwer, K. Inoue, R.J. Voll, L.J. Young, and M.M. Goodman Synthesis and evaluation of C-11, F-18 and I-125 small molecule radioligands for detecting oxytocin receptors Bioorg. Med. Chem. 20 2012 2721 2738
90. S.E. Taylor, G.C. Gonzaga, L.C. Klein, P. Hu, G.A. Greendale, and T.E. Seeman Relation of oxytocin to psychological stress responses and hypothalamic-pituitary-adrenocortical axis activity in older women Psychosom. Med. 68 2006 238 245
91. S.E. Taylor, S. Saphire-Bernstein, and T.E. Seeman Are plasma oxytocin in women and plasma vasopressin in men biomarkers of distressed pair-bond relationships? Psychol. Sci. 21 2010 3 7
92. A. Theodoridou, A.C. Rowe, I.S. Penton-Voak, and P.J. Rogers Oxytocin and social perception: oxytocin increases perceived facial trustworthiness and attractiveness Horm. Behav. 56 2009 128 132
93. R.R. Thompson, K. George, J.C. Walton, S.P. Orr, and J. Benson Sex-specific influences of vasopressin on human social communication Proc. Natl. Acad. Sci. U. S. A. 103 2006 7889 7894
94. R.G. Thorne, G.J. Pronk, V. Padmanabhan, and W.H. Frey 2nd Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration Neuroscience 127 2004 481 496
95. D.M. Toloczko, L. Young, and T.R. Insel Are there oxytocin receptors in the primate brain? Ann. N. Y. Acad. Sci. 807 1997 506 509
96. C. Unkelbach, A.J. Guastella, and J.P. Forgas Oxytocin selectively facilitates recognition of positive sex and relationship words Psychol. Sci. 19 2008 1092 1094
97. J.G. Veening, T. de Jong, and H.P. Barendregt Oxytocin-messages via the cerebrospinal fluid: behavioral effects; a review Physiol. Behav. 101 2010 193 210
98. C. Viero, I. Shibuya, N. Kitamura, A. Verkhratsky, H. Fujihara, A. Katoh, Y. Ueta, H.H. Zingg, A. Chvatal, E. Sykova, and G. Dayanithi REVIEW: Oxytocin: crossing the bridge between basic science and pharmacotherapy CNS Neurosci. Ther. 16 2010 e138 156
99. J.R. Williams, T.R. Insel, C.R. Harbaugh, and C.S. Carter Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster) J. Neuroendocrinol. 6 1994 247 250
100. J.T. Winslow, P.L. Noble, C.K. Lyons, S.M. Sterk, and T.R. Insel Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys Neuropsychopharmacology 28 2003 910 918
101. J.S. Winston, B.A. Strange, J. O'Doherty, and R.J. Dolan Automatic and intentional brain responses during evaluation of trustworthiness of faces Nat. Neurosci. 5 2002 277 283
102. L.J. Young, B. Huot, R. Nilsen, Z. Wang, and T.R. Insel Species differences in central oxytocin receptor gene expression: comparative analysis of promoter sequences J. Neuroendocrinol. 8 1996 777 783
103. P.J. Zak, R. Kurzban, and W.T. Matzner Oxytocin is associated with human trustworthiness Horm. Behav. 48 2005 522 527
104. P.J. Zak, A.A. Stanton, and S. Ahmadi Oxytocin increases generosity in humans PLoS One 2 2007 e1128