Effects of intranasal oxytocin administration on memory for infant cues: Moderation by childhood emotional maltreatment

Social Neuroscience

Volumn 9, Issue 5, 2014, Pages 536-547

  Bhandari, Ritu ^a   van der Veen, Rixt ^a   Parsons, Christine E ^b   Young, Katherine S ^b   Voorthuis, Alexandra ^a   Bakermans Kranenburg, Marian J ^a   Stein, Alan ^b   Kringelbach, Morten L ^b   van IJzendoorn, Marinus H ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Baby Social Reward Task; Decision making; Emotional maltreatment; Intranasal administration; Memory; Oxytocin

Indexed keywords

CENTRAL NERVOUS SYSTEM AGENTS; OXYTOCIN;

ASSOCIATION; CHILD ABUSE; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; EMOTION; FACIAL EXPRESSION; FEMALE; HUMAN; INFANT; INTRANASAL DRUG ADMINISTRATION; LEARNING; MEMORY; PATTERN RECOGNITION; PERCEPTION; PHYSIOLOGY; PSYCHOLOGIC TEST; PSYCHOLOGY; QUESTIONNAIRE; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; YOUNG ADULT;

ADMINISTRATION, INTRANASAL; CENTRAL NERVOUS SYSTEM AGENTS; CHILD ABUSE; CUES; DOUBLE-BLIND METHOD; EMOTIONS; FACIAL EXPRESSION; FEMALE; HUMANS; INFANT; LEARNING; MEMORY; OXYTOCIN; PATTERN RECOGNITION, VISUAL; PSYCHOLOGICAL TESTS; QUESTIONNAIRES; REACTION TIME; SOCIAL PERCEPTION; YOUNG ADULT;

EID: 84904721225     PISSN: 17470919     EISSN: 17470927     Source Type: Journal    
DOI: 10.1080/17470919.2014.932307     Document Type: Article

References (55)

1. Bakermans-Kranenburg, M. J., & Van IJzendoorn, M. H. (2013). Sniffing around oxytocin: Review and meta-analyses of trials in healthy and clinical groups with implications for pharmacotherapy. Translational Psychiatry, 3, e258. doi:10.1038/tp.2013.34
2. Bakermans-Kranenburg, M. J., Van Ijzendoorn, M. H., Riem, M. M. E., Tops, M., & Alink, L. R. A. (2012). Oxytocin decreases handgrip force in reaction to infant crying in females without harsh parenting experiences. Social Cognitive and Affective Neuroscience, 7(8), 951-957. doi:10.1093/scan/nsr067
3. Bartz, J. A., Zaki, J., Ochsner, K. N., Bolger, N., Kolevzon, A., Ludwig, N., & Lydon, J. E. (2010). Effects of oxytocin on recollections of maternal care and closeness. Proceedings of the National Academy of Sciences, 107(50), 21371-21375. doi:10.1073/pnas.1012669107
4. Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T.,. Zule, W. (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse & Neglect, 27(2), 169-190. doi:10.1016/S0145-2134(02)00541-0
5. Bhandari, R., Bakermans-Kranenburg, M. J., Van Der Veen, R., Parsons, C. E., Young, K. S., Grewen, K. M.,. Van IJzendoorn, M. H. (2014). Salivary oxytocin mediates the association between emotional maltreatment and responses to emotional infant faces. Physiology & Behavior, 131, 123-128. doi:10.1016/j.physbeh.2014.04.028
6. Blandón-Gitlin, I., Pezdek, K., Saldivar, S., & Steelman, E. (2013). Oxytocin eliminates the own-race bias in face recognition memory. Brain Research. Advance online publication. doi:10.1016/j.brainres.2013.07.015
7. Carpenter, L. L., Tyrka, A. R., Ross, N. S., Khoury, L., Anderson, G. M., & Price, L. H. (2009). Effect of childhood emotional abuse and age on cortisol responsivity in adulthood. Biological Psychiatry, 66(1), 69-75. doi:10.1016/j.biopsych.2009.02.030
8. Clark-Elford, R., Nathan, P. J., Auyeung, B., Voon, V., Sule, A., Müller, U.,. Baron-Cohen, S. (2014). The effects of oxytocin on social reward learning in humans. The International Journal of Neuropsychopharmacology, 17(2), 199-209. doi:10.1017/S1461145713001120
9. Crawford, J. R., & Henry, J. D. (2004). The positive and negative affect schedule (PANAS): Construct validity, measurement properties and normative data in a large non-clinical sample. British Journal of Clinical Psychology, 43(3), 245-265. doi:10.1348/0144665031752934
10. De Dreu, C. K. W., Greer, L. L., Handgraaf, M. J. J., Shalvi, S., & Van Kleef, G. A. (2012). Oxytocin modulates selection of allies in intergroup conflict. Proceedings of the Royal Society B: Biological Sciences, 279(1731), 1150-1154. doi:10.1098/rspb.2011.1444
11. De Dreu, C. K. W., Greer, L. L., Handgraaf, M. J. J., Shalvi, S., Van Kleef, G. A., Baas, M.,. Feith, S. W. W. (2010). The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science, 328(5984), 1408-1411. doi:10.1126/science.1189047
12. 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. doi:10.1016/j.biopsych.2008.10.011
13. Feldman, R., Gordon, I., & Zagoory-Sharon, O. (2011). Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: Considering stress and affiliation components of human bonding. Developmental Science, 14(4), 752-761. doi:10.1111/j.1467-7687.2010.01021.x
14. Feldman, R., Weller, A., Zagoory-Sharon, O., & Levine, A. (2007). Evidence for a neuroendocrinological foundation of human affiliation: Plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychological Science, 18(11), 965-970. doi:10.1111/j.1467-9280.2007.02010.x
15. Fischer-Shofty, M., Levkovitz, Y., & Shamay-Tsoory, S. G. (2012). Oxytocin facilitates accurate perception of competition in men and kinship in women. Social Cognitive and Affective Neuroscience, 8(3), 313-317. doi:10.1093/scan/nsr100
16. Glocker, M. L., Langleben, D. D., Ruparel, K., Loughead, J. W., Valdez, J. N., Griffin, M. D.,. Gur, R. C. (2009). Baby schema modulates the brain reward system in nulliparous women. Proceedings of the National Academy of Sciences, 106(22), 9115-9119. doi:10.1073/pnas.0811620106
17. Grimm, S., Pestke, K., Feeser, M., Aust, S., Weigand, A., Wang, J.,. Bajbouj, M. (2014). Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress. Social Cognitive and Affective Neuroscience. Advance online publication. doi:10.1093/scan/nsu020
18. Guastella, A. J., & Macleod, C. (2012). A critical review of the influence of oxytocin nasal spray on social cognition in humans: Evidence and future directions. Hormones and Behavior, 61(3), 410-418. doi:10.1016/j.yhbeh.2012.01.002
19. Guastella, A. J., Mitchell, P. B., & Mathews, F. (2008). Oxytocin enhances the encoding of positive social memories in humans. Biological Psychiatry, 64(3), 256-258. doi:10.1016/j.biopsych.2008.02.008
20. Heim, C., Young, L. J., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2009). Lower CSF oxytocin concentrations in women with a history of childhood abuse. Molecular Psychiatry, 14(10), 954-958. doi:10.1038/mp.2008.112
21. Heinrichs, M., Meinlschmidt, G., Wippich, W., Ehlert, U., & Hellhammer, D. H. (2004). Selective amnesic effects of oxytocin on human memory. Physiology & Behavior, 83(1), 31-38. doi:10.1016/j.physbeh.2004.07.020
22. Heinrichs, M., Von Dawans, B., & Domes, G. (2009). Oxytocin, vasopressin, and human social behavior. Frontiers in Neuroendocrinology, 30(4), 548-557. doi:10.1016/j.yfrne.2009.05.005
23. Herzmann, G., Young, B., Bird, C. W., & Curran, T. (2012). Oxytocin can impair memory for social and non-social visual objects: A within-subject investigation of oxytocin's effects on human memory. Brain Research, 1451(0), 65-73. doi:10.1016/j.brainres.2012.02.049
24. Huffmeijer, R., Alink, L. R., Tops, M., Bakermans-Kranenburg, M. J., & Van IJzendoorn, M. H. (2012). Asymmetric frontal brain activity and parental rejection predict altruistic behavior: Moderation of oxytocin effects. Cognitive, Affective & Behavioral Neuroscience, 12(2), 382-392. doi:10.3758/s13415-011-0082-6.
25. Kirsch, P., Esslinger, C., Chen, Q., Mier, D., Lis, S., Siddhanti, S., & Meyer-Lindenberg, A. (2005). Oxytocin modulates neural circuitry for social cognition and fear in humans. The Journal of Neuroscience, 25(49), 11489-11493. doi:10.1523/jneurosci.3984-05.2005
26. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005). Oxytocin increases trust in humans. Nature, 435(7042), 673-676. doi:10.1038/nature03701
27. Kovács, G. L., Bohus, B., Versteeg, D. H. G., Ronald De Kloet, E., & De Wied, D. (1979). Effect of oxytocin and vasopressin on memory consolidation: Sites of action and catecholaminergic correlates after local microinjection into limbic-midbrain structures. Brain Research, 175(2), 303-314. doi:10.1016/0006-8993(79)91009-6
28. Kovacs, G. L., & Telegdy, G. (1982). Role of oxytocin in memory and amnesia. Pharmacology & Therapeutics, 18(3), 375-395. doi:10.1016/0163-7258(82)90038-9
29. Kringelbach, M. L., Lehtonen, A., Squire, S., Harvey, A. G., Craske, M. G., Holliday, I. E.,. Fitch, T. (2008). A specific and rapid neural signature for parental instinct. Plos ONE, 3(2), e1664. doi:10.1371/journal.pone.0001664
30. Linnen, A.-M., Ellenbogen, M. A., Cardoso, C., & Joober, R. (2012). Intranasal oxytocin and salivary cortisol concentrations during social rejection in university students. Stress (Amsterdam, Netherlands), 15(4), 393-402. doi:10.3109/10253890.2011.631154
31. Macdonald, K. S. (2013). Sex, receptors and attachment: A review of individual factors influencing response to oxytocin. Frontiers in Neuroscience, 6, 194. doi:10.3389/fnins.2012.00194
32. Marsh, A., Yu, H., Pine, D., Gorodetsky, E., Goldman, D., & Blair, R. J. R. (2012). The influence of oxytocin administration on responses to infant faces and potential moderation by OXTR genotype. Psychopharmacology, 224(4), 469-476. doi:10.1007/s00213-012-2775-0
33. Naber, F., Poslawsky, I., Van IJzendoorn, M. H., Engeland, H., & Bakermans-Kranenburg, M. (2013). Brief report: Oxytocin enhances paternal sensitivity to a child with autism: A double-blind within-subject experiment with intranasally administered oxytocin. Journal of Autism and Developmental Disorders, 43(1), 224-229. doi:10.1007/s10803-012-1536-6
34. Parsons, C. E., Young, K. S., Bhandari, R., Van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Stein, A., & Kringelbach, M. L. (2014). The bonnie baby: Experimentally manipulated temperament affects perceived cuteness and motivation to view infant faces. Developmental Science, 17(2), 257-269. doi:10.1111/desc.12112
35. Pierrehumbert, B., Torrisi, R., Laufer, D., Halfon, O., Ansermet, F., & Beck Popovic, M. (2010). Oxytocin response to an experimental psychosocial challenge in adults exposed to traumatic experiences during childhood or adolescence. Neuroscience, 166(1), 168-177. doi:10.1016/j.neuroscience.2009.12.016
36. Pine, D. S., Mogg, K., Bradley, B. P., Montgomery, L., Monk, C. S., Mcclure, E., & Kaufman, J. (2005). Attention bias to threat in maltreated children: Implications for vulnerability to stress-related psychopathology. American Journal of Psychiatry, 162(2), 291-296. doi:10.1176/appi.ajp.162.2.291
37. Radke, S., Roelofs, K., & De Bruijn, E. R. A. (2013). Acting on anger: Social anxiety modulates approach-avoidance tendencies after oxytocin administration. Psychological Science, 24(8), 1573-1578. doi:10.1177/0956797612472682
38. Riem, M. M., Bakermans-Kranenburg, M. J., Voorthuis, A., & Van IJzendoorn, M. H. (2014). Oxytocin effects on mind-reading are moderated by experiences of maternal love withdrawal: An fMRI study. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 51(51), 105-112. doi:10.1016/j.pnpbp.2014.01.014.
39. Riem, M. M. E., Bakermans-Kranenburg, M. J., Huffmeijer, R., & Van IJzendoorn, M. H. (2013). Does intranasal oxytocin promote prosocial behavior to an excluded fellow player? A randomized-controlled trial with Cyberball. Psychoneuroendocrinology, 38(8), 1418-1425. doi:10.1016/j.psyneuen.2012.12.023
40. Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M.,. Rombouts, S. A. (2011). Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: A randomized controlled trial. Biological Psychiatry, 70(3), 291-297. doi:10.1016/j.biopsych.2011.02.006
41. Rimmele, U., Hediger, K., Heinrichs, M., & Klaver, P. (2009). Oxytocin makes a face in memory familiar. The Journal of Neuroscience, 29(1), 38-42. doi:10.1523/jneurosci.4260-08.2009
42. Savaskan, E., Ehrhardt, R., Schulz, A., Walter, M., & Schächinger, H. (2008). Post-learning intranasal oxytocin modulates human memory for facial identity. Psychoneuroendocrinology, 33(3), 368-374. doi:10.1016/j.psyneuen.2007.12.004
43. Seltzer, L. J., Ziegler, T., Connolly, M. J., Prososki, A. R., & Pollak, S. D. (2014). Stress-induced elevation of oxytocin in maltreated children: Evolution, neurodevelopment, and social behavior. Child Development, 85(2), 501-512. doi:10.1111/cdev.12136
44. Smeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008). True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology, 33(10), 1378-1386. doi:10.1016/j.psyneuen.2008.07.009
45. Sroufe, L. A. (2005). Attachment and development: A prospective, longitudinal study from birth to adulthood. Attachment & Human Development, 7(4), 349-367. doi:10.1080/14616730500365928
46. Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 34(13), 2655-2666. doi:10.1038/npp.2009.103. Retrieved from http://www.nature.com/npp/journal/v34/n13/suppinfo/npp2009103s1.html
47. 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. doi:10.1016/j.yfrne.2011.07.001
48. Van Harmelen, A.-L., Elzinga, B. M., Kievit, R. A., & Spinhoven, P. (2011). Intrusions of autobiographical memories in individuals reporting childhood emotional maltreatment. European Journal of Psychotraumatology, 2. doi:10.3402/ejpt.v2i0.7336
49. Van Harmelen, A. L., Van Tol, M. J., Dalgleish, T., Van Der Wee, N. J., Veltman, D. J., Aleman, A.,. Elzinga, B. M. (2014). Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience. Advance online publication. doi:10.1093/scan/nsu008
50. Van Harmelen, A.-L., Van Tol, M.-J., Demenescu, L. R., Van Der Wee, N. J. A., Veltman, D. J., Aleman, A., & Elzinga, B. M. (2012). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience, 8(4), 362-369. doi:10.1093/scan/nss007
51. Van IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2012). A sniff of trust: Meta-analysis of the effects of intranasal oxytocin administration on face recognition, trust to in-group, and trust to out-group. Psychoneuroendocrinology, 37(3), 438-443. doi:10.1016/j.psyneuen.2011.07.008
52. Van IJzendoorn, M. H., Bhandari, R., Van Der Veen, R., Grewen, K., & Bakermans-Kranenburg, M. J. (2012). Elevated salivary levels of oxytocin persist more than seven hours after intranasal administration. Frontiers in Neuroscience, 6, 174. doi:10.3389/fnins.2012.00174
53. Van IJzendoorn, M. H., Huffmeijer, R., Alink, L. R. A., Bakermans-Kranenburg, M. J., & Tops, M. (2011). The impact of oxytocin administration on charitable donating is moderated by experiences of parental love-withdrawal. Frontiers in Psychology, 2, 258. doi:10.3389/fpsyg.2011.00258
54. Weigand, A., Feeser, M., Gärtner, M., Brandt, E., Fan, Y., Fuge, P.,. Grimm, S. (2013). Effects of intranasal oxytocin prior to encoding and retrieval on recognition memory. Psychopharmacology, 227(2), 321-329. doi:10.1007/s00213-012-2962-z
55. Young, K. S., Parsons, C. E., Stein, A., & Kringelbach, M. L. (2012). Interpreting infant vocal distress: The ameliorative effect of musical training in depression. Emotion (Washington, D.C.), 12(6), 1200-1205. doi:10.1037/a0028705