Abstract
Rationale
Oxytocin is a neuropeptide that is associated with increases in social affiliative behaviors, particularly toward infants. However, no previous study has investigated healthy adults’ responses to infant faces following oxytocin administration. In addition, given that preliminary evidence suggests that a single-nucleotide polymorphism of the oxytocin receptor (OXTR) gene, rs53576, may influence behaviors associated with parental sensitivity, we assessed whether such responses vary according to OXTR rs53576 genotype.
Objectives
The present study assessed the effects of intranasally administered oxytocin and OXTR genotype on human adults’ preferences for infant faces.
Methods
A double-blind, between-groups design was used, with 57 genotyped volunteers randomly assigned to receive intranasally administered oxytocin or placebo. Fifty minutes following the administration of oxytocin or placebo, participants viewed infants’ and adults’ faces showing neutral expressions and assessed how appealing they found each face.
Results
Infants’ faces were more strongly preferred following oxytocin inhalation relative to placebo. When participants were separated according to genotype, this effect was only observed for participants homozygous for the rs53576G allele. Parallel effects were not seen for adults’ faces.
Conclusions
The present results are consistent with the hypothesis that acute oxytocin administration increases sensitivity to reward-relevant features of infants and/or reduces sensitivity to their aversive properties. The results are also consistent with suggestions of more efficient oxytocinergic function in rs53576G homozygotes.
Similar content being viewed by others
References
Bakermans-Kranenburg MJ, Van Ijzendoorn MH (2008) Oxytocin receptor (oxtr) and serotonin transporter (5-htt) genes associated with observed parenting. Soc Cogn Affect Neurosci 3:128–134. doi:10.1093/scan/nsn004
Bartz J, Zaki J, Bolger N, Hollander E, Ludwig N, Kolevzon A, Ochsner K (2010) Oxytocin selectively improves empathic accuracy. Psychol Sci 21:1426–1428. doi:10.1177/0956797610383439
Bartz J, Simeon D, Hamilton H, Kim S, Crystal S, Braun A, Vicens V, Hollander E (2011) Oxytocin can hinder trust and cooperation in borderline personality disorder. Soc Cogn Affect Neurosci 6:556–563. doi:10.1093/scan/nsq085
Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E (2008) Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58:639–650. doi:10.1016/j.neuron.2008.04.009
Carter CS (1998) Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23:779–818. doi:10.1016/S0306-4530(98)00055-9
Carter CS, Altemus M (1997) Integrative functions of lactational hormones in social behavior and stress management. Ann N Y Acad Sci 807:164–174. doi:10.1111/j.1749-6632.1997.tb51918.x
Champagne F, Diorio J, Sharma S, Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci 98:12736-12741. doi:10.1073/pnas.221224598
Chen F, Barth M, Johnson S, Gotlib I, Johnson S (2011) Oxytocin receptor (OXTR) polymorphisms and attachment in human infants. Front Psychol 2:200. doi:10.3389/fpsyg.2011.00200
Costa B, Pini S, Gabelloni P, Abelli M, Lari L, Cardini A, Muti M, Gesi C, Landi S, Galderisi S, Mucci A, Lucacchini A, Cassano G, Martini C (2009) Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology 34:1506–1514. doi:10.1016/j.psyneuen.2009.05.006
De Dreu CK (2012) Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda. Horm Behav 61:419–428. doi:10.1016/j.yhbeh.2011.12.009
De Waal FB (2008) Putting the altruism back into altruism: the evolution of empathy. Annu Rev Psychol 59:279–300. doi:10.1146/annurev.psych.59.103006.093625
Ebstein RP, Israel S, Chew SH, Zhong S, Knafo A (2010) Genetics of human social behavior. Neuron 65(6):831–844. doi:10.1016/j.neuron.2010.02.020
Eibl-Eibesfeldt I (1996) Love and hate: the natural history of behavior patterns. Aldine, Venice
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. Psychol Sci 18:965–970. doi:10.1111/j.1467-9280.2007.02010.x
Fewtrell M, Loh K, Blake A, Ridout D, Hawdon J (2006) Randomised, double blind trial of oxytocin nasal spray in mothers expressing breast milk for preterm infants. Arch Dis Child Fetal Neonatal Ed 91:F169–74. doi:10.1136/adc.2005.081265
Fleming A, Vaccarino F, Luebke C (1980) Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav 25:731–743
Forsling ML (1986) Regulation of oxytocin release. In: Gantner D, Pfaff D (eds) Current topics in neuroendocrinology, vol. 6, neurobiology of oxytocin. Springer, Berlin
Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145–1148. doi:10.1046/j.1365-2826.2000.00599.x
Francis DD, Young LJ, Meaney MJ, Insel TR (2002) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (v1a) receptors: gender differences. J Neuroendocrinol 14:349–353. doi:10.1046/j.0007-1331.2002.00776.x
Grosvenor CE, Shah GV, Crowley WR (1990) Role of neurogenic stimuli and milk production in the regulation of prolactin secretion during lactation. In: Krasnegor NA, Bridges RS (eds) Mammalian parenting: biochemical, neurobiological, and behavioral determinants. Oxford University Press, New York, pp 324–342
Guastella A, Kemp A (2011) The role of oxytocin in human affect: a novel hypothesis. Curr Dir Psychol Sci 20:222–231. doi:10.1177/0963721411417547
Heekeren HR, Wartenburger I, Schmidt H, Prehn K, Schwintowski HP, Villringer A (2005) Influence of bodily harm on neural correlates of semantic and moral decision-making. Neuroimage 24:887–897. doi:10.1016/j.neuroimage.2004.09.026
Insel TR (1992) Oxytocin—a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 17:3–35. doi:10.1016/0306-4530(92)90073-G
Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65(6):768–779. doi:10.1016/j.neuron.2010.03.005
Kendrick KM (1997) Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res Bull 44:383–395. doi:10.1016/S0361-9230(97)00218-9
Kendrick KM, Keverne EB, Baldwin BA (1987) Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 46:56–61. doi:10.1159/000124796
Kogan A, Saslow L, Impett E, Oveis C, Keltner D, Rodrigues Saturn S (2011) Thin-slicing study of the oxytocin receptor (OXTR) gene and the evaluation and expression of the prosocial disposition. Proc Natl Acad Sci U S A 108:19189–19192. doi:10.1073/pnas.1112658108
Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673–676. doi:10.1038/nature03701
Labuschagne I, Phan K, Wood A, Angstadt M, Chua P, Heinrichs M, Stout J, Nathan P (2010) Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 35:2403–2413. doi:10.1038/npp.2010.123
Leng G, Meddle S, Douglas A (2008) Oxytocin and the maternal brain. Curr Opin Pharmacol 8:731–734. doi:10.1016/j.coph.2008.07.001
Madden JR, Clutton-Brock TH (2011) Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal. Proc Biol Sci 278:1189–1194. doi:10.1098/rspb.2010.1675
Marsh AA, Yu HH, Schechter JC, Blair RJR (2009) Larger than life: humans' nonverbal status cues alter perceived size. PLoS One 4:e5707. doi:10.1371/journal.pone.0005707
Marsh AA, Yu HH, Pine D, Blair R (2010) Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology 209:225–232. doi:10.1007/s00213-010-1780-4
Naber F, Van Ijzendoorn MH, Deschamps P, Van Engeland H, Bakermans-Kranenburg MJ (2010) Intranasal oxytocin increases fathers' observed responsiveness during play with their children: a double-blind within-subject experiment. Psychoneuroendocrinology 35:1583–1586. doi:10.1016/j.psyneuen.2010.04.007
Pedersen CA (2004) Biological aspects of social bonding and the roots of human violence. Ann N Y Acad Sci 1036:106–127. doi:10.1196/annals.1330.006
Pedersen CA, Ascher JA, Monroe YL, Prange AJJ (1982) Oxytocin induces maternal behavior in virgin female rats. Science 216:648–650
Pedersen CA, Caldwell JD, Peterson G, Walker CH, Mason GA (1992) Oxytocin activation of maternal behavior in the rat. Ann N Y Acad Sci 652:58–69. doi:10.1111/j.1749-6632.1992.tb34346.x
Razzoli M, Cushing B, Carter C, Valsecchi P (2003) Hormonal regulation of agonistic and affiliative behavior in female Mongolian gerbils (Meriones unguiculatus). Horm Behav 43:549–553. doi:10.1016/S0018-506X(03)00064-3
Riem M, Bakermans-Kranenburg MJ, Pieper S, Tops M, Boksem M, Vermeiren R, Van Ijzendoorn MH, Rombouts S (2011) Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol Psychiatry 70:291–297. doi:10.1016/j.biopsych.2011.02.006
Rockliff H, Karl A, McEwan K, Gilbert J, Matos M, Gilbert P (2011) Effects of intranasal oxytocin on compassion focused imagery. Emotion 11: 1388-1396. doi:10.1037/a0023861
Rodrigues S, Saslow L, Garcia N, John O, Keltner D (2009) Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc Natl Acad Sci U S A 106:21437–21441. doi:10.1073/pnas.0909579106
Ross H, Freeman S, Spiegel L, Ren X, Terwilliger E, Young L (2009) Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. J Neurosci 29:1312–1318. doi:10.1523/JNEUROSCI.5039-08.2009
Shamay-Tsoory SG, Fischer M, Dvash J, Harari H, Perach-Bloom N, Levkovitz Y (2009) Intranasal administration of oxytocin increases envy and schadenfreude (gloating). Biol Psychiatry 66:864–870. doi:10.1016/j.biopsych.2009.06.009
Strathearn L, Fonagy P, Amico J, Montague P (2009) Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 34:2655–2666. doi:10.1038/npp.2009.103
Swain J, Tasgin E, Mayes LC, Feldman R, Todd Constable R, Leckman J (2008) Maternal brain response to own baby-cry is affected by cesarean section delivery. J Child Psychol Psychiatry 49:1042–1052. doi:10.1111/j.1469-7610.2008.01963.x
Tansey KE, Brookes K, Hill M, Cochrane L, Gill M, Skuse D, Correia C, Vicente A, Kent L, Gallagher L, Anney R (2010) Oxytocin receptor (OXTR) does not play a major role in the aetiology of autism: genetic and molecular studies. Neurosci Lett 474:163–167. doi:10.1016/j.neulet.2010.03.035
Tops M, Van Ijzendoorn MH, Riem M, Boksem M, Bakermans-Kranenburg MJ (2011) Oxytocin receptor gene associated with the efficiency of social auditory processing. Front Psychiatry 2:60. doi:10.3389/fpsyt.2011.00060
Tost H, Kolachana B, Hakimi S, Lemaitre H, Verchinski B, Mattay V, Weinberger D, Meyer-Lindenberg A (2010) A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic–limbic structure and function. Proc Natl Acad Sci U S A 107:13936–13941. doi:10.1073/pnas.1003296107
Toth A, Varala K, Newman T, Miguez F, Hutchison S, Willoughby D, Simons J, Egholm M, Hunt J, Hudson M, Robinson G (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318:441–444. doi:10.1126/science.1146647
Wechsler D (1999) Wechsler abbreviated scale of intelligence. Psychological Corporation, San Antonio
Wu S, Jia M, Ruan Y, Liu J, Guo Y, Shuang M, Gong X, Zhang Y, Yang X, Zhang D (2005) Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biol Psychiatry 58:74–77. doi:10.1016/j.biopsych.2005.03.013
Young LJ, Lim MM, Gingrich B, Insel TR (2001) Cellular mechanisms of social attachment. Horm Behav 40:133–138. doi:10.1006/hbeh.2001.1691
Zak P, Stanton A, Ahmadi S (2007) Oxytocin increases generosity in humans. PLoS One 2:e1128. doi:10.1371/journal.pone.0001128
Zebrowitz LA, Luevano VX, Bronstad PM, Aharon I (2009) Neural activation to babyfaced men matches activation to babies. Soc Neurosci 4:1–10. doi:10.1080/17470910701676236
Acknowledgments
This research was supported by the Intramural Research Program of the NIH/NIMH. The authors would like to thank Andy Speer, Samantha Crowe, Nanette Schell, David Fink, Adriana Pavletic, and Judith Starling for their assistance in conducting this research.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marsh, A.A., Yu, H.H., Pine, D.S. et al. The influence of oxytocin administration on responses to infant faces and potential moderation by OXTR genotype. Psychopharmacology 224, 469–476 (2012). https://doi.org/10.1007/s00213-012-2775-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-012-2775-0