Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans

Brain Imaging and Behavior

Volumn 9, Issue 4, 2015, Pages 754-764

  Feng, Chunliang ^a   Hackett, Patrick D ^a   DeMarco, Ashley C ^c   Chen, Xu ^a,b   Stair, Sabrina ^b   Haroon, Ebrahim ^b   Ditzen, Beate ^a,b,d   Pagnoni, Giuseppe ^e   Rilling, James K ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS   (United States)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Cooperation; fMRI; Oxytocin; Sex differences; Vasopressin

Indexed keywords

OXYTOCIN; PLACEBO; VASOPRESSIN; OXYGEN; PSYCHOTROPIC AGENT; VASOPRESSIN DERIVATIVE;

AMYGDALOID NUCLEUS; ARTICLE; BOLD SIGNAL; CAUDATE NUCLEUS; CINGULATE GYRUS; CONTROLLED STUDY; COOPERATION; CORPUS STRIATUM; DOUBLE BLIND PROCEDURE; FEMALE; FOREBRAIN; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; INSULA; MAJOR CLINICAL STUDY; MALE; MEDIAL FRONTAL CORTEX; MIDDLE FRONTAL GYRUS; NERVE POTENTIAL; POSTCENTRAL GYRUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PUTAMEN; RANDOMIZED CONTROLLED TRIAL; SEX DIFFERENCE; SEXUAL BEHAVIOR; SOCIAL INTERACTION; SUPRAMARGINAL GYRUS; TEMPORAL GYRUS; THALAMUS; ADOLESCENT; BLOOD; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; COMPARATIVE STUDY; DRUG EFFECTS; INTRANASAL DRUG ADMINISTRATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PRISONER DILEMMA; REWARD; SEXUAL DEVELOPMENT; YOUNG ADULT;

ADMINISTRATION, INTRANASAL; ADOLESCENT; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; COOPERATIVE BEHAVIOR; DOUBLE-BLIND METHOD; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; OXYTOCIN; PRISONER DILEMMA; PSYCHOTROPIC DRUGS; REWARD; SEX CHARACTERISTICS; VASOPRESSINS; YOUNG ADULT;

EID: 84948574467     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-014-9333-9     Document Type: Article

References (63)

1. Albers, H. E. (2012). The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network. Hormones and Behavior, 61(3), 283–292.
2. Altemus, M., Jacobson, K. R., Debellis, M., Kling, M., Pigott, T., Murphy, D. L., et al. (1999). Normal CSF oxytocin and NPY levels in OCD. Biological Psychiatry, 45(7), 931–933.
3. Amodio, D. M., & Frith, C. D. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7(4), 268–277.
4. Andari, E., Duhamel, J.-R., Zalla, T., Herbrecht, E., Leboyer, M., & Sirigu, A. (2010). Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proceedings of the National Academy of Sciences, 107(9), 4389–4394.
5. Avinun, R., Israel, S., Shalev, I., Gritsenko, I., Bornstein, G., Ebstein, R. P., et al. (2011). AVPR1A variant associated with preschoolers’ lower altruistic behavior. PloS One, 6(9), e25274.
6. Bales, K. L., & Carter, C. S. (2003). Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles Microtus ochrogaster. Hormones and Behavior, 44(3), 178–184.
7. Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011). Social effects of oxytocin in humans: context and person matter. Trends in Cognitive Sciences, 15(7), 301–309.
8. Boccia, M., Petrusz, P., Suzuki, K., Marson, L., & Pedersen, C. (2013). Immunohistochemical localization of oxytocin receptors in human brain. Neuroscience, 253, 155–164.
9. Campbell, A., Ruffman, T., Murray, J., & Glue, P. (2014). Oxytocin improves emotion recognition for older males. Neurobiology of Aging (ahead-of-print), 1–13.
10. Cardoso, C., Ellenbogen, M. A., Orlando, M. A., Bacon, S. L., & Joober, R. (2013). Intranasal oxytocin attenuates the cortisol response to physical stress: a dose–response study. Psychoneuroendocrinology, 38(3), 399–407.
11. Cardoso, C., Orlando, M. A., Brown, C. A., & Ellenbogen, M. A. (2014). Oxytocin and enhancement of the positive valence of social affiliation memories: An autobiographical memory study. Social neuroscience (ahead-of-print), 1–10.
12. Coccaro, E. F., Kavoussi, R. J., Hauger, R. L., Cooper, T. B., & Ferris, C. F. (1998). Cerebrospinal fluid vasopressin levels: correlates with aggression and serotonin function in personality-disordered subjects. Archives of General Psychiatry, 55(8), 708–714.
13. De Dreu, C. K. (2012). Oxytocin modulates the link between adult attachment and cooperation through reduced betrayal aversion. Psychoneuroendocrinology, 37(7), 871–880.
14. 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(9), 728–731.
15. Dodhia, S., Hosanagar, A., Fitzgerald, D. A., Labuschagne, I., Wood, A. G., Nathan, P. J., et al. (2014). Modulation of Resting-State Amygdala-Frontal Functional Connectivity by Oxytocin in Generalized Social Anxiety Disorder. Neuropsychopharmacology (ahead of print).
16. Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007). Oxytocin improves “mind-reading” in humans. Biological Psychiatry, 61(6), 731–733.
17. Dumais, K. M., Bredewold, R., Mayer, T. E., & Veenema, A. H. (2013). Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region-and sex-specific ways. Hormones and Behavior, 64(4), 693–701.
18. Ebstein, R. P., Israel, S., Chew, S. H., Zhong, S., & Knafo, A. (2010). Genetics of human social behavior. Neuron, 65(6), 831–844.
19. Fischer-Shofty, M., Levkovitz, Y., & Shamay-Tsoory, S. G. (2013). Oxytocin facilitates accurate perception of competition in men and kinship in women. Social Cognitive and Affective Neuroscience, 8(3), 313–317.
20. Goodson, J. L., & Thompson, R. R. (2010). Nonapeptide mechanisms of social cognition, behavior and species-specific social systems. Current Opinion in Neurobiology, 20(6), 784–794.
21. Gordon, I., Vander Wyk, B. C., Bennett, R. H., Cordeaux, C., Lucas, M. V., Eilbott, J. A., et al. (2013). Oxytocin enhances brain function in children with autism. Proceedings of the National Academy of Sciences, 110(52), 20953–20958.
22. Greve, D. N., & Fischl, B. (2009). Accurate and robust brain image alignment using boundary-based registration. NeuroImage, 48(1), 63–72.
23. Guastella, A. J., Einfeld, S. L., Gray, K. M., Rinehart, N. J., Tonge, B. J., Lambert, T. J., et al. (2010a). Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biological Psychiatry, 67(7), 692–694.
24. Guastella, A. J., Kenyon, A. R., Alvares, G. A., Carson, D. S., & Hickie, I. B. (2010b). Intranasal arginine vasopressin enhances the encoding of happy and angry faces in humans. Biological Psychiatry, 67(12), 1220–1222.
25. Guastella, A. J., Kenyon, A. R., Unkelbach, C., Alvares, G. A., & Hickie, I. B. (2011). Arginine Vasopressin selectively enhances recognition of sexual cues in male humans. Psychoneuroendocrinology, 36(2), 294–297.
26. Güroğlu, B., van den Bos, W., van Dijk, E., Rombouts, S. A., & Crone, E. A. (2011). Dissociable brain networks involved in development of fairness considerations: understanding intentionality behind unfairness. NeuroImage, 57(2), 634–641.
27. Harlé, K. M., Chang, L. J., van’t Wout, M., & Sanfey, A. G. (2012). The neural mechanisms of affect infusion in social economic decision-making: a mediating role of the anterior insula. NeuroImage, 61(1), 32–40.
28. Heinrichs, M., von Dawans, B., & Domes, G. (2009). Oxytocin, vasopressin, and human social behavior. Frontiers in Neuroendocrinology, 30(4), 548–557.
29. Hoge, E. A., Anderson, E., Lawson, E. A., Bui, E., Fischer, L. E., Khadge, S. D., et al. (2014). Gender moderates the effect of oxytocin on social judgments. Human Psychopharmacology: Clinical and Experimental, 29(3), 299–304.
30. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841.
31. King-Casas, B., Tomlin, D., Anen, C., Camerer, C. F., Quartz, S. R., & Montague, P. R. (2005). Getting to know you: reputation and trust in a two-person economic exchange. Science, 308(5718), 78–83.
32. Knafo, A., Israel, S., Darvasi, A., Bachner-Melman, R., Uzefovsky, F., Cohen, L., et al. (2008). 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 and Behavior, 7(3), 266–275.
33. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005). Oxytocin increases trust in humans. Nature, 435(7042), 673–676.
34. Krueger, F., Grafman, J., & McCabe, K. (2008). Neural correlates of economic game playing. Philosophical Transactions of the Royal Society, B: Biological Sciences, 363(1511), 3859–3874.
35. Labuschagne, I., Phan, K. L., Wood, A., Angstadt, M., Chua, P., Heinrichs, M., et al. (2010). Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology, 35(12), 2403–2413.
36. Liu, Y., & Wang, Z. (2003). Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience, 121(3), 537–544.
37. Loup, F., Tribollet, E., Dubois-Dauphin, M., & Dreifuss, J. (1991). Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Research, 555(2), 220–232.
38. Lynn, S. K., Hoge, E. A., Fischer, L. E., Barrett, L. F., & Simon, N. M. (2014). Gender differences in oxytocin-associated disruption of decision bias during emotion perception. Psychiatry Research (ahead of print), 1–22.
39. Macdonald, K., & Feifel, D. (2013). Helping oxytocin deliver: considerations in the development of oxytocin-based therapeutics for brain disorders. Frontiers in Neuroscience, 7(35), 1–21.
40. Marsh, A. A., Henry, H. Y., Pine, D. S., & Blair, R. (2010). Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology, 209(3), 225–232.
41. Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function, 214(5–6), 655–667.
42. 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(9), 524–538.
43. Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., & Landgraf, R. (2013). Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology, 38(10), 1985–1993.
44. Preckel, K., Scheele, D., Kendrick, K. M., Maier, W., & Hurlemann, R. (2014). Oxytocin facilitates social approach behavior in women. Frontiers in Behavioral Neuroscience, 8(191), 1–9.
45. Rilling, J. K., & Sanfey, A. G. (2011). The neuroscience of social decision-making. Annual Review of Psychology, 62, 23–48.
46. Rilling, J. K., Gutman, D. A., Zeh, T. R., Pagnoni, G., Berns, G. S., & Kilts, C. D. (2002). A neural basis for social cooperation. Neuron, 35(2), 395–405.
47. Rilling, J. K., Sanfey, A. G., Aronson, J. A., Nystrom, L. E., & Cohen, J. D. (2004). The neural correlates of theory of mind within interpersonal interactions. NeuroImage, 22(4), 1694–1703.
48. Rilling, J. K., DeMarco, A. C., Hackett, P. D., Thompson, R., Ditzen, B., Patel, R., et al. (2012). Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology, 37(4), 447–461.
49. Rilling, J. K., DeMarco, A. C., Hackett, P. D., Chen, X., Gautam, P., Stair, S., et al. (2014). Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction. Psychoneuroendocrinology, 39, 237–248.
50. Ross, H. E., & Young, L. J. (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Frontiers in Neuroendocrinology, 30(4), 534–547.
51. Shahrestani, S., Kemp, A. H., & Guastella, A. J. (2013). The impact of a single administration of intranasal oxytocin on the recognition of basic emotions in humans: a meta-analysis. Neuropsychopharmacology, 38(10), 1929–1936.
52. Skuse, D. H., & Gallagher, L. (2009). Dopaminergic-neuropeptide interactions in the social brain. Trends in Cognitive Science, 13(1), 27–35.
53. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155.
54. Sørensen, P., Gjerris, A., & Hammer, M. (1985). Cerebrospinal fluid vasopressin in neurological and psychiatric disorders. Journal of Neurology, Neurosurgery & Psychiatry, 48(1), 50–57.
55. Striepens, N., Kendrick, K. M., Maier, W., & Hurlemann, R. (2011). Prosocial effects of oxytocin and clinical evidence for its therapeutic potential. Frontiers in Neuroendocrinology, 32(4), 426–450.
56. Striepens, N., Kendrick, K. M., Hanking, V., Landgraf, R., Wüllner, U., Maier, W., et al. (2013). Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans. Scientific Reports, 3(3440), 1–5.
57. Thompson, R., George, K., Walton, J., Orr, S., & Benson, J. (2006). Sex-specific influences of vasopressin on human social communication. Proceedings of the National Academy of Sciences, 103(20), 7889–7894.
58. Veenema, A. H., Bredewold, R., & De Vries, G. J. (2013). Sex-specific modulation of juvenile social play by vasopressin. Psychoneuroendocrinology, 38(11), 2554–2561.
59. Watanabe, T., Abe, O., Kuwabara, H., Yahata, N., Takano, Y., Iwashiro, N., et al. (2014). Mitigation of sociocommunicational deficits of autism through oxytocin-induced recovery of medial prefrontal activity: a randomized trial. JAMA Psychiatry, 71(2), 166–175.
60. Woo, C.-W., Krishnan, A., & Wager, T. D. (2014). Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. NeuroImage, 91, 412–419.
61. Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage, 14(6), 1370–1386.
62. Young, L. J., Murphy Young, A. Z., & Hammock, E. A. (2005). Anatomy and neurochemistry of the pair bond. Journal of Comparative Neurology, 493(1), 51–57.
63. Zink, C. F., Pagnoni, G., Martin-Skurski, M. E., Chappelow, J. C., & Berns, G. S. (2004). Human striatal responses to monetary reward depend on saliency. Neuron, 42(3), 509–517.