Plasma oxytocin explains individual differences in neural substrates of social perception

Frontiers in Human Neuroscience

Volumn 9, Issue MAR, 2015, Pages

  Lancaster, Katie ^a   Carter, C Sue ^b   Pournajafi Nazarloo, Hossein ^b   Karaoli, Themistoclis ^c   Lillard, Travis S ^a   Jack, Allison ^d   Davis, John M ^e   Morris, James P ^a   Connelly, Jessica J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

fMRI; Individual differences; Neuroendocrinology; Neuroimaging; Oxytocin; Social cognition

Indexed keywords

OXYTOCIN;

ADULT; ANATOMICAL VARIATION; ARTICLE; BLOOD SAMPLING; BRAIN REGION; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HORMONE DETERMINATION; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; MALE; MEDIAL PREFRONTAL CORTEX; NEUROANATOMY; OXYTOCIN BLOOD LEVEL; PREDICTION; PREFRONTAL CORTEX; SOCIAL COGNITION; SUPERIOR TEMPORAL GYRUS; TEMPORAL SULCUS; TEMPOROPARIETAL JUNCTION; VENTRAL MEDIAL PREFRONTAL CORTEX;

EID: 84933674152     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2015.00132     Document Type: Article

References (42)

1. Abell, F., Happé, F., and Frith, U. (2000). Do triangles play tricks? Attribution of mental states to animated shapes in normal and abnormal development. Cogn. Dev. 15, 1-16. doi: 10.1016/s0885-2014(00)00014-9
2. Atzil, S., Hendler, T., Zagoory-Sharon, O., Winetraub, Y., and Feldman, R. (2012). Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin. J. Am. Acad. Child Adolesc. Psychiatry 51, 798-811. doi: 10.1016/j.jaac.2012.06.008
3. Bartz, J. A., Zaki, J., Bolger, N., Hollander, E., Ludwig, N. N., Kolevzon, A., et al. (2010). Oxytocin selectively improves empathic accuracy. Psychol. Sci. 21, 1426-1428. doi: 10.1177/0956797610383439
4. Bartz, J. A., Zaki, J., Bolger, N., and Ochsner, K. N. (2011). Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 15, 301-309. doi: 10.1016/j.tics.2011.05.002
5. Bethlehem, R. A. I., van Honk, J., Auyeung, B., and Baron-Cohen, S. (2013). Oxytocin, brain physiology and functional connectivity: a review of intranasal oxytocin fMRI studies. Psychoneuroendocrinology 38, 962-974. doi: 10.1016/j.psyneuen.2012.10.011
6. Cardoso, C., Ellenbogen, M. A., Orlando, M. A., Bacon, S. L., and Joober, R. (2013). Intranasal oxytocin attenuates the cortisol response to physical stress: a dose-response study. Psychoneuroendocrinology 38, 399-407. doi: 10.1016/j.psyneuen.2012.07.013
7. Carter, C. S., Pournajafi-Nazarloo, H., Kramer, K. M., Ziegler, T. E., White-Traut, R., Bello, D., et al. (2007). Oxytocin: behavioral associations and potential as a salivary biomarker. Ann. N Y Acad. Sci. 1098, 312-322. doi: 10.1196/annals.1384.006
8. Castelli, F., Frith, C., Happé, F., and Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain 125, 1839-1849. doi: 10.1093/brain/awf189
9. Castelli, F., Happé, F., Frith, U., and Frith, C. (2000). Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage 12, 314-325. doi: 10.1006/nimg.2000.0612
10. Domes, G., Heinrichs, M., Michel, A., Berger, C., and Herpertz, S. C. (2007). Oxytocin improves "mind-reading" in humans. Biol. Psychiatry 61, 731-733. doi: 10.1016/j.biopsych.2006.07.015
11. 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. doi: 10.1016/j.psyneuen.2009.06.016
12. Evans, S. L., Dal Monte, O., Noble, P., and Averbeck, B. B. (2014). Intranasal oxytocin effects on social cognition: a critique. Brain Res. 1580, 69-77. doi: 10.1016/j.brainres.2013.11.008
13. Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., and Zagoory-Sharon, O. (2010). Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact.Psychoneuroendocrinology 35, 1133-1141. doi: 10.1016/j.psyneuen.2010.01.013
14. Feldman, R., Weller, A., Zagoory-Sharon, O., and Levine, A. (2007). Evidence for a neuroendocrinological foundation of human affiliation plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol. Sci. 18, 965-970. doi: 10.1111/j.1467-9280.2007.02010.x
15. Gordon, I., Zagoory-Sharon, O., Leckman, J. F., and Feldman, R. (2010). Oxytocin and the development of parenting in humans. Biol. Psychiatry 68, 377-382. doi: 10.1016/j.biopsych.2010.02.005
16. Gouin, J.-P., Carter, C. S., Pournajafi-Nazarloo, H., Glaser, R., Malarkey, W. B., Loving, T. J., et al. (2010). Marital behavior, oxytocin, vasopressin and wound healing. Psychoneuroendocrinology 35, 1082-1090. doi: 10.1016/j.psyneuen.2010.01.009
17. Guastella, A. J., Einfeld, S. L., Gray, K. M., Rinehart, N. J., Tonge, B. J., Lambert, T. J., et al. (2010). Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol. Psychiatry 67, 692-694. doi: 10.1016/j.biopsych.2009.09.020
18. Heider, F., and Simmel, M. (1944). An experimental study of apparent behavior. Am. J. Psychol. 57, 243-259. doi: 10.2307/1416950
19. Kaiser, M. D., Hudac, C. M., Shultz, S., Lee, S. M., Cheung, C., Berken, A. M., et al. (2010). Neural signatures of autism. Proc. Natl. Acad. Sci. U S A 107, 21223-21228. doi: 10.1073/pnas.1010412107
20. Kéri, S., and Benedek, G. (2009). Oxytocin enhances the perception of biological motion in humans. Cogn. Affect. Behav. Neurosci. 9, 237-241. doi: 10.3758/cabn.9.3.237
21. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., and Fehr, E. (2005). Oxytocin increases trust in humans.Nature 435, 673-676. doi: 10.1038/nature03701
22. Kramer, K. M., Cushing, B. S., Carter, C. S., Wu, J., and Ottinger, M. A. (2004). Sex and species differences in plasma oxytocin using an enzyme immunoassay. Can. J. Zool. 82, 1194-1200. doi: 10.1139/z04-098
23. Landgraf, R., and Neumann, I. D. (2004). Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 25, 150-176. doi: 10.1016/j.yfrne.2004.05.001
24. MacDonald, E., Dadds, M. R., Brennan, J. L., Williams, K., Levy, F., and Cauchi, A. J. (2011). A review of safety, side-effects and subjective reactions to intranasal oxytocin in human research. Psychoneuroendocrinology 36, 1114-1126. doi: 10.1016/j.psyneuen.2011.02.015
25. Marsh, A. A., Yu, H. H., Pine, D. S., and Blair, R. J. R. (2010). Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology (Berl) 209, 225-232. doi: 10.1007/s00213-010-1780-4
26. Martin, W. L., and Carter, C. S. (2013). Oxytocin and vasopressin are sequestered in plasma. Presented at the 10th World Congress on Neurohypophysial Hormones. Bristol, England.
27. McCarthy, M. M., and Pfaus, J. G. (1996). Steroid modulation of neurotransmitter function to alter female reproductive behavior. Trends Endocrinol. Metab. 7, 327-333. doi: 10.1016/s1043-2760(96)00157-9
28. Modahl, C., Green, L. A., Fein, D., Morris, M., Waterhouse, L., Feinstein, C., et al. (1998). Plasma oxytocin levels in autistic children. Biol. Psychiatry 43, 270-277. doi: 10.1016/s0006-3223(97)00439-3
29. Neumann, I. D. (2008). Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J. Neuroendocrinol. 20, 858-865. doi: 10.1111/j.1365-2826.2008.01726.x
30. Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., and Landgraf, R. (2013). Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology 38, 1985-1993. doi: 10.1016/j.psyneuen.2013.03.003
31. Parker, K. J., Garner, J. P., Libove, R. A., Hyde, S. A., Hornbeak, K. B., Carson, D. S., et al. (2014). Plasma oxytocin concentrations and OXTR polymorphisms predict social impairments in children with and without autism spectrum disorder. Proc. Natl. Acad. Sci. U S A 111, 12258-12263. doi: 10.1073/pnas.1402236111
32. Rubin, L. H., Carter, C. S., Bishop, J. R., Pournajafi-Nazarloo, H., Drogos, L. L., Hill, S. K., et al. (2014). Reduced levels of vasopressin and reduced behavioral modulation of oxytocin in psychotic disorders. Schizophr. Bull. 40, 1374-1384. doi: 10.1093/schbul/sbu027
33. Rubin, L. H., Carter, C. S., Drogos, L., Pournajafi-Nazarloo, H., Sweeney, J. A., and Maki, P. M. (2010). Peripheral oxytocin is associated with reduced symptom severity in schizophrenia. Schizophr. Res. 124, 13-21. doi: 10.1016/j.schres.2010.09.014
34. Salonia, A., Nappi, R. E., Pontillo, M., Daverio, R., Smeraldi, A., Briganti, A., et al. (2005). Menstrual cycle-related changes in plasma oxytocin are relevant to normal sexual function in healthy women. Horm. Behav. 47, 164-169. doi: 10.1016/j.yhbeh.2004.10.002
35. Schultz, R. T., Grelotti, D. J., Klin, A., Kleinman, J., Van der Gaag, C., Marois, R., et al. (2003). The role of the fusiform face area in social cognition: implications for the pathobiology of autism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 415-427. doi: 10.1098/rstb.2002.1208
36. Tavares, P., Lawrence, A. D., and Barnard, P. J. (2008). Paying attention to social meaning: an fMRI study. Cereb. Cortex 18, 1876-1885. doi: 10.1093/cercor/bhm212
37. Tops, M., Van Peer, J. M., Korf, J., Wijers, A. A., and Tucker, D. M. (2007). Anxiety, cortisol and attachment predict plasma oxytocin. Psychophysiology 44, 444-449. doi: 10.1111/j.1469-8986.2007.00510.x
38. Winslow, J. T., Noble, P. L., Lyons, C. K., Sterk, S. M., and Insel, T. R. (2003). Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology 28, 910-918. doi: 10.1038/sj.npp.1300128
39. Worsley, K. J. (2001). "Statistical analysis of activation images," in Functional MRI: An Introduction to Methods, eds P. Jezzard, P. Matthews and S. Smith (New York: Oxford University Press), 251-270.
40. Zak, P. J., Stanton, A. A., and Ahmadi, S. (2007). Oxytocin increases generosity in humans. PLoS One 2:e1128. doi: 10.1371/journal.pone.0001128
41. Zaki, J., and Ochsner, K. N. (2012). The neuroscience of empathy: progress, pitfalls and promise. Nat. Neurosci. 15, 675-680. doi: 10.1038/nn.3085
42. Zhong, S., Monakhov, M., Mok, H. P., Tong, T., Lai, P. S., Chew, S. H., et al. (2012). U-shaped relation between plasma oxytocin levels and behavior in the trust game. PLoS One 7:e51095. doi: 10.1371/journal.pone.0051095