Effects of oxytocin on recollections of maternal care and closeness

Edited by Shelley E. Taylor, University of California, Los Angeles, CA, and approved October 28, 2010 (received for review August 26, 2010)
November 29, 2010
107 (50) 21371-21375

Abstract

Although the infant–caregiver attachment bond is critical to survival, little is known about the biological mechanisms supporting attachment representations in humans. Oxytocin plays a key role in attachment bond formation and maintenance in animals and thus could be expected to affect attachment representations in humans. To investigate this possibility, we administered 24 IU intranasal oxytocin to healthy male adults in a double-blind, placebo-controlled, crossover designed study and then assessed memories of childhood maternal care and closeness—two features of the attachment bond. We found that the effects of oxytocin were moderated by the attachment representations people possess, with less anxiously attached individuals remembering their mother as more caring and close after oxytocin (vs. placebo) but more anxiously attached individuals remembering their mother as less caring and close after oxytocin (vs. placebo). These data contrast with the popular notion that oxytocin has broad positive effects on social perception and are more consistent with the animal literature, which emphasizes oxytocin's role in encoding social memories and linking those memories to the reward value of the social stimulus.

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Acknowledgments

We thank Julian Beale, Cara Settipani, Katherine Remy, Ana Tryfon, David Grodberg, and Khalid Khan for research assistance. The Beatrice and Samuel A. Seaver Foundation provided financial support.

References

1
M Mikulincer, PR Shaver, The attachment behavioral system in adulthood: Activation, psychodynamics, and interpersonal processes. Advances in Experimental Social Psychology, ed MP Zanna (Academic Press, New York) 35, 53–152 (2003).
2
J Bowlby Attachment and Loss, Volume 1. Attachment (Basic Books, New York, 1969).
3
M Mikulincer, PR Shaver Attachment in Adulthood: Structure, Dynamics, and Change (Guilford, New York, 2007).
4
JP Burbach, LJ Young, J Russell, Oxytocin: Synthesis, secretion, and reproductive functions. Knobil and Neill's Physiology of Reproduction, ed JD Neill (Elsevier, New York), pp. 3055–3128 (2006).
5
CS Carter, Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23, 779–818 (1998).
6
TR Insel, LJ Young, The neurobiology of attachment. Nat Rev Neurosci 2, 129–136 (2001).
7
J Panksepp, Oxytocin effects on emotional processes: Separation distress, social bonding, and relationships to psychiatric disorders. Ann N Y Acad Sci 652, 243–252 (1992).
8
HE Ross, LJ Young, Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30, 534–547 (2009).
9
TR Insel, Is social attachment an addictive disorder? Physiol Behav 79, 351–357 (2003).
10
M Kosfeld, M Heinrichs, PJ Zak, U Fischbacher, E Fehr, Oxytocin increases trust in humans. Nature 435, 673–676 (2005).
11
PJ Zak, AA Stanton, S Ahmadi, Oxytocin increases generosity in humans. PLoS ONE 2, e1128 (2007).
12
PJ Zak, R Kurzban, WT Matzner, Oxytocin is associated with human trustworthiness. Horm Behav 48, 522–527 (2005).
13
RA Thompson, Early sociopersonality development. Handbook of Child Psychology: Social, Emotional, and Personality Development, eds W Damon, N Eisenberg (John Wiley & Sons, 5th Ed, New York) 3, 25–104 (1998).
14
RC Fraley, Attachment stability from infancy to adulthood: Meta-analysis and dynamic modeling of developmental mechanisms. Pers Soc Psychol Rev 6, 123–151 (2002).
15
JA Bartz, E Hollander, The neuroscience of affiliation: Forging links between basic and clinical research on neuropeptides and social behavior. Horm Behav 50, 518–528 (2006).
16
K Wilhelm, H Niven, G Parker, D Hadzi-Pavlovic, The stability of the Parental Bonding Instrument over a 20-year period. Psychol Med 35, 387–393 (2005).
17
AJ Guastella, PB Mitchell, F Mathews, Oxytocin enhances the encoding of positive social memories in humans. Biol Psychiatry 64, 256–258 (2008).
18
U Rimmele, K Hediger, M Heinrichs, P Klaver, Oxytocin makes a face in memory familiar. J Neurosci 29, 38–42 (2009).
19
E Savaskan, R Ehrhardt, A Schulz, M Walter, H Schächinger, Post-learning intranasal oxytocin modulates human memory for facial identity. Psychoneuroendocrinology 33, 368–374 (2008).
20
Z Kunda, The case for motivated reasoning. Psychol Bull 108, 480–498 (1990).
21
J Metcalfe, W Mischel, A hot/cool-system analysis of delay of gratification: Dynamics of willpower. Psychol Rev 106, 3–19 (1999).
22
LJ Levine, MA Safer, Sources of bias in memory for emotions. Curr Dir Psychol Sci 11, 169–173 (2002).
23
O Ayduk, W Mischel, G Downey, Attentional mechanisms linking rejection to hostile reactivity: The role of “hot” versus “cool” focus. Psychol Sci 13, 443–448 (2002).
24
RH Fazio, DM Sanbonmatsu, MC Powell, FR Kardes, On the automatic activation of attitudes. J Pers Soc Psychol 50, 229–238 (1986).
25
NC Overall, GJO Fletcher, MD Friesen, Mapping the intimate relationship mind: Comparisons between three models of attachment representations. Pers Soc Psychol Bull 29, 1479–1493 (2003).
26
T Pierce, JE Lydon, Global and specific relational models in the experience of social interactions. J Pers Soc Psychol 80, 613–631 (2001).
27
KA Brennan, CL Clark, PR Shaver, Self-report measurement of adult attachment: An integrative overview. Attachment Theory and Close Relationships, eds JA Simpson, WS Rholes (Guilford Press, New York), pp. 46–76 (1998).
28
DM McNair, M Lorr, LF Dropplemanm EdiITS Manual for the Profile of Mood States (Educational & Industrial Testing Service, San Diego, CA, 1992).
29
JA Bartz, et al., Oxytocin selectively improves empathic accuracy. Psychol Sci 21, 1426–1428 (2010).
30
G Parker, H Tupling, LB Brown, A parental bonding instrument. Br J Med Psychol 52, 1–10 (1979).
31
A Aron, EN Aron, M Tudor, G Nelson, Close relationships as including other in the self. J Pers Soc Psychol 60, 241–253 (1991).
32
M Rosenberg Society and the Adolescent Self-Image (Princeton Univ Press, Princeton, 1965).
33
K Bartholomew, LM Horowitz, Attachment styles among young adults: A test of a four-category model. J Pers Soc Psychol 61, 226–244 (1991).
34
G Parker, The Parental Bonding Instrument: Psychometric properties reviewed. Psychiatr Dev 7, 317–335 (1989).
35
M Uji, N Tanaka, M Shono, T Kitamura, Factorial structure of the parental bonding instrument (PBI) in Japan: A study of cultural, developmental, and gender influences. Child Psychiatry Hum Dev 37, 115–132 (2006).
36
RC Fraley, PR Shaver, Adult attachment and the suppression of unwanted thoughts. J Pers Soc Psychol 73, 1080–1091 (1997).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 107 | No. 50
December 14, 2010
PubMed: 21115834

Classifications

Submission history

Published online: November 29, 2010
Published in issue: December 14, 2010

Keywords

  1. neurohypophyseal hormones
  2. social cognition
  3. social memory
  4. individual differences
  5. Syntocinon

Acknowledgments

We thank Julian Beale, Cara Settipani, Katherine Remy, Ana Tryfon, David Grodberg, and Khalid Khan for research assistance. The Beatrice and Samuel A. Seaver Foundation provided financial support.

Notes

*This Direct Submission article had a prearranged editor.
There was a significant effect of drug administration order on change in maternal closeness ratings [b = −0.79, t(26) = −2.29, P < 0.05] but not on change in maternal care ratings (t < 0.5). Importantly, additional analyses showed no order × attachment anxiety interaction (t < 0.5), indicating that the effect of attachment anxiety on change in maternal closeness ratings does not depend on drug administration order.

Authors

Affiliations

Jennifer A. Bartz1 [email protected]
Department of Psychiatry, Mount Sinai School of Medicine, New York, NY 10029;
Jamil Zaki
Department of Psychology, Harvard University, Cambridge, MA 02138;
Kevin N. Ochsner
Department of Psychology, Columbia University, New York, NY 10027; and
Niall Bolger
Department of Psychology, Columbia University, New York, NY 10027; and
Alexander Kolevzon
Department of Psychiatry, Mount Sinai School of Medicine, New York, NY 10029;
Natasha Ludwig
Department of Psychiatry, Mount Sinai School of Medicine, New York, NY 10029;
John E. Lydon
Department of Psychology, McGill University, Montreal, QC, Canada H3A 2T5

Notes

1
To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: J.A.B. designed research; J.A.B., A.K., and N.L. performed research; J.A.B. and N.B. analyzed data; and J.A.B., J.Z., K.N.O., N.B., and J.E.L. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Effects of oxytocin on recollections of maternal care and closeness
    Proceedings of the National Academy of Sciences
    • Vol. 107
    • No. 50
    • pp. 21231-21943

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