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Intranasal oxytocin increases covert attention to positive social cues

Published online by Cambridge University Press:  12 November 2012

G. Domes ,
M. Sibold ,
L. Schulze ,
A. Lischke ,
S. C. Herpertz  and
M. Heinrichs
G. Domes*
Affiliation:
Department of Psychology, University of Freiburg, Germany Freiburg Brain Imaging Center, University Medical Center, University of Freiburg, Germany
M. Sibold
Affiliation:
Department of Psychology, University of Freiburg, Germany
L. Schulze
Affiliation:
Department of Educational Sciences and Psychology, Freie Universität Berlin, Germany
A. Lischke
Affiliation:
Department of General Psychiatry, University of Heidelberg, Germany Department of Psychiatry and Psychotherapy, University of Rostock, Germany
S. C. Herpertz
Affiliation:
Department of Psychiatry and Psychotherapy, University of Rostock, Germany
M. Heinrichs
Affiliation:
Department of Psychology, University of Freiburg, Germany Freiburg Brain Imaging Center, University Medical Center, University of Freiburg, Germany
*
*Address for correspondence: G. Domes, Ph.D., Department of Psychology, Laboratory for Biological and Personality Psychology, University of Freiburg, Stefan-Meier-Strasse 8, D-79104 Freiburg, Germany. (Email: domes@psychologie.uni-freiburg.de)
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Abstract

Background

The neuropeptide oxytocin (OT) has positive effects on the processing of emotional stimuli such as facial expressions. To date, research has focused primarily on conditions of overt visual attention.

Method

We investigated whether a single intranasal dose of OT (24 IU) would modulate the allocation of attentional resources towards positive and negative facial expressions using a dot-probe paradigm in a sample of 69 healthy men. Attentional capacity for these facial cues was limited by presentation time (100 or 500 ms). In addition, we controlled for overt visual attention by recording eye movements using a remote eye tracker.

Results

Reaction times (RTs) in the dot-probe paradigm revealed a pronounced shift of attention towards happy facial expressions presented for 100 ms after OT administration, whereas there were no OT-induced effects for longer presentation times (500 ms). The results could not be attributed to modulations of overt visual attention as no substance effects on gazes towards the facial target were observed.

Conclusions

The results suggest that OT increased covert attention to happy faces, thereby supporting the hypothesis that OT modulates early attentional processes that might promote prosocial behavior.

Keywords

Attentionawarenesseye trackingfacial emotionsneuropeptidesoxytocin
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 8 , August 2013 , pp. 1747 - 1753
Copyright
Copyright © Cambridge University Press 2012 

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References

Alvares, GA, Chen, NT, Balleine, BW, Hickie, IB, Guastella, AJ (2012). Oxytocin selectively moderates negative cognitive appraisals in high trait anxious males. Psychoneuroendocrinology. Published online: 20 05 2012. doi:10.1016/j.psyneuen.2012.04.018.CrossRefGoogle ScholarPubMed
Bar-Haim, Y, Lamy, D, Pergamin, L, Bakermans-Kranenburg, MJ, van IJzendoorn, MH (2007). Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychological Bulletin 133, 1–24.CrossRefGoogle ScholarPubMed
Baskerville, TA, Douglas, AJ (2010). Dopamine and oxytocin interactions underlying behaviors: potential contributions to behavioral disorders. CNS Neuroscience and Therapeutics 16, e92–e123.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Born, J, Lange, T, Kern, W, McGregor, GP, Bickel, U, Fehm, HL (2002). Sniffing neuropeptides: a transnasal approach to the human brain. Nature Neuroscience 5, 514–516.CrossRefGoogle ScholarPubMed
Calamaras, MR, Tone, EB, Anderson, PL (2012). A pilot study of attention bias subtypes: examining their relation to cognitive bias and their change following cognitive behavioral therapy. Journal of Clinical Psychology. Published online: 18 05 2012. doi:10.1002/jclp.21875.CrossRefGoogle ScholarPubMed
Campbell, DB, Datta, D, Jones, ST, Batey Lee, E, Sutcliffe, JS, Hammock, EA, Levitt, P (2011). Association of oxytocin receptor (OXTR) gene variants with multiple phenotype domains of autism spectrum disorder. Journal of Neurodevelopmental Disorders 3, 101–112.CrossRefGoogle ScholarPubMed
Cooper, RM, Langton, SRH (2006). Attentional bias to angry faces using the dot-probe task? It depends when you look for it. Behaviour Research and Therapy 44, 1321–1329.CrossRefGoogle Scholar
Dai, L, Carter, CS, Ying, J, Bellugi, U, Pournajafi-Nazarloo, H, Korenberg, JR (2012). Oxytocin and vasopressin are dysregulated in Williams Syndrome, a genetic disorder affecting social behavior. PLoS ONE 7, e38513.CrossRefGoogle ScholarPubMed
Davis, M, Whalen, PJ (2001). The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13–34.CrossRefGoogle ScholarPubMed
Di Simplicio, M, Massey-Chase, R, Cowen, P, Harmer, C (2009). Oxytocin enhances processing of positive versus negative emotional information in healthy male volunteers. Journal of Psychopharmacology 23, 241–248.CrossRefGoogle ScholarPubMed
Dodd, HF, Porter, MA (2010). I see happy people: attention bias towards happy but not angry facial expressions in Williams syndrome. Cognitive Neuropsychiatry 15, 549–567.CrossRefGoogle Scholar
Domes, G, Heinrichs, M, Glascher, J, Buchel, C, Braus, DF, Herpertz, SC (2007 a). Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biological Psychiatry 62, 1187–1190.CrossRefGoogle ScholarPubMed
Domes, G, Heinrichs, M, Michel, A, Berger, C, Herpertz, SC (2007 b). Oxytocin improves ‘mind-reading’ in humans. Biological Psychiatry 61, 731–733.CrossRefGoogle ScholarPubMed
Domes, G, Lischke, A, Berger, C, Grossmann, A, Hauenstein, K, Heinrichs, M, Herpertz, SC (2010). Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35, 83–93.CrossRefGoogle ScholarPubMed
Ellenbogen, MA, Linnen, AM, Grumet, R, Cardoso, C, Joober, R (2012). The acute effects of intranasal oxytocin on automatic and effortful attentional shifting to emotional faces. Psychophysiology 49, 128–137.CrossRefGoogle ScholarPubMed
Fischer-Shofty, M, Shamay-Tsoory, SG, Harari, H, Levkovitz, Y (2010). The effect of intranasal administration of oxytocin on fear recognition. Neuropsychologia 48, 179–184.CrossRefGoogle ScholarPubMed
Franke, G (1995). The Symptom Checklist by Derogatis – German Version – SCL-90-R [in German]. Beltz: Göttingen.Google Scholar
Gamer, M, Zurowski, B, Buchel, C (2010). Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proceedings of the National Academy of Sciences USA 107, 9400–9405.CrossRefGoogle ScholarPubMed
Guastella, AJ, Einfeld, SL, Gray, KM, Rinehart, NJ, Tonge, BJ, Lambert, TJ, Hickie, IB (2010). Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biological Psychiatry 67, 692–694.CrossRefGoogle ScholarPubMed
Guastella, AJ, Howard, AL, Dadds, MR, Mitchell, P, Carson, DS (2009). A randomized controlled trial of intranasal oxytocin as an adjunct to exposure therapy for social anxiety disorder. Psychoneuroendocrinology 34, 917–923.CrossRefGoogle ScholarPubMed
Guastella, AJ, Mitchell, PB, Dadds, MR (2008). Oxytocin increases gaze to the eye region of human faces. Biological Psychiatry 63, 3–5.CrossRefGoogle Scholar
Heinrichs, M, Domes, G (2008). Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans. Progress in Brain Research 170, 337–350.CrossRefGoogle ScholarPubMed
Heinrichs, M, von Dawans, B, Domes, G (2009). Oxytocin, vasopressin, and human social behavior. Frontiers in Neuroendocrinology 30, 548–557.CrossRefGoogle ScholarPubMed
Jarvinen-Pasley, A, Vines, BW, Hill, KJ, Yam, A, Grichanik, M, Mills, D, Reiss, AL, Korenberg, JR, Bellugi, U (2010). Cross-modal influences of affect across social and non-social domains in individuals with Williams syndrome. Neuropsychologia 48, 456–466.CrossRefGoogle ScholarPubMed
Jones, W, Bellugi, U, Lai, Z, Chiles, M, Reilly, J, Lincoln, A, Adolphs, R (2000). II. Hypersociability in Williams Syndrome. Journal of Cognitive Neuroscience 12 (Suppl. 1), 30–46.CrossRefGoogle ScholarPubMed
Keebaugh, AC, Young, LJ (2011). Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Hormones and Behavior 60, 498–504.CrossRefGoogle ScholarPubMed
Kirsch, P, Esslinger, C, Chen, Q, Mier, D, Lis, S, Siddhanti, S, Gruppe, H, Mattay, VS, Gallhofer, B, Meyer-Lindenberg, A (2005). Oxytocin modulates neural circuitry for social cognition and fear in humans. Journal of Neuroscience 25, 11489–11493.CrossRefGoogle ScholarPubMed
Kliemann, D, Dziobek, I, Hatri, A, Steimke, R, Heekeren, HR (2010). Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. Journal of Neuroscience 30, 12281–12287.CrossRefGoogle ScholarPubMed
Krebs, RM, Boehler, CN, Roberts, KC, Song, AW, Woldorff, MG (2012). The involvement of the dopaminergic midbrain and cortico-striatal-thalamic circuits in the integration of reward prospect and attentional task demands. Cerebral Cortex 22, 607–615.CrossRefGoogle ScholarPubMed
Kumsta, R, Heinrichs, M (2012). Oxytocin, stress and social behavior: neurogenetics of the human oxytocin system. Current Opinions in Neurobiology. Published online: 03 10 2012. doi:10.1016/j.conb.2012.09.004.Google ScholarPubMed
Leknes, S, Wessberg, J, Ellingsen, DM, Chelnokova, O, Olausson, H, Laeng, B (2012). Oxytocin enhances pupil dilation and sensitivity to ‘hidden’ emotional expressions. Social Cognitive and Affective Neuroscience. Published online: 29 06 2012. doi:10.1093/scan/nss062.Google ScholarPubMed
Lischke, A, Berger, C, Prehn, K, Heinrichs, M, Herpertz, SC, Domes, G (2012 a). Intranasal oxytocin enhances emotion recognition from dynamic facial expressions and leaves eye-gaze unaffected. Psychoneuroendocrinology 37, 475–481.CrossRefGoogle ScholarPubMed
Lischke, A, Gamer, M, Berger, C, Grossmann, A, Hauenstein, K, Heinrichs, M, Herpertz, SC, Domes, G (2012 b). Oxytocin increases amygdala reactivity to threatening scenes in females. Psychoneuroendocrinology 37, 1431–1438.CrossRefGoogle ScholarPubMed
Lundqvist, D, Flykt, A, Ohman, A (1998). The Karolinska Directed Emotional Faces (KDEF). Department of Neurosciences, Karolinska Hospital: Stockholm.Google Scholar
MacLeod, C, Mathews, A, Tata, P (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology 95, 15–20.CrossRefGoogle ScholarPubMed
Marsh, AA, Yu, HH, Pine, DS, Blair, RJ (2010). Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology 209, 225–232.CrossRefGoogle ScholarPubMed
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, 524–538.CrossRefGoogle ScholarPubMed
Mogg, K, Bradley, BP (2002). Selective orienting of attention to masked threat faces in social anxiety. Behaviour Research and Therapy 40, 1403–1414.CrossRefGoogle ScholarPubMed
Moore, DJ, Heavey, L, Reidy, J (2012). Attentional processing of faces in ASD: a dot-probe study. Journal of Autism and Developmental Disorders 42, 2038–2045.CrossRefGoogle ScholarPubMed
Pedersen, CA, Gibson, CM, Rau, SW, Salimi, K, Smedley, KL, Casey, RL, Leserman, J, Jarskog, LF, Penn, DL (2011). Intranasal oxytocin reduces psychotic symptoms and improves Theory of Mind and social perception in schizophrenia. Schizophrenia Research 132, 50–53.CrossRefGoogle ScholarPubMed
Pobbe, RL, Pearson, BL, Defensor, EB, Bolivar, VJ, Young, WS 3rd, Lee, HJ, Blanchard, DC, Blanchard, RJ (2012). Oxytocin receptor knockout mice display deficits in the expression of autism-related behaviors. Hormones and Behavior 61, 436–444.CrossRefGoogle ScholarPubMed
Porter, MA, Shaw, TA, Marsh, PJ (2010). An unusual attraction to the eyes in Williams-Beuren syndrome: a manipulation of facial affect while measuring face scanpaths. Cognitive Neuropsychiatry 15, 505–530.CrossRefGoogle Scholar
Riby, DM, Hancock, PJ (2009). Do faces capture the attention of individuals with Williams syndrome or autism? Evidence from tracking eye movements. Journal of Autism and Developmental Disorders 39, 421–431.CrossRefGoogle ScholarPubMed
Sauer, C, Montag, C, Worner, C, Kirsch, P, Reuter, M (2012). Effects of a common variant in the CD38 gene on social processing in an oxytocin challenge study: possible links to autism. Neuropsychopharmacology 37, 1474–1482.CrossRefGoogle Scholar
Schulze, L, Lischke, A, Greif, J, Herpertz, SC, Heinrichs, M, Domes, G (2011). Oxytocin increases recognition of masked emotional faces. Psychoneuroendocrinology 36, 1378–1382.CrossRefGoogle ScholarPubMed
Shahrokh, DK, Zhang, TY, Diorio, J, Gratton, A, Meaney, MJ (2010). Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151, 2276–2286.CrossRefGoogle ScholarPubMed
Shechner, T, Britton, JC, Perez-Edgar, K, Bar-Haim, Y, Ernst, M, Fox, NA, Leibenluft, E, Pine, DS (2012). Attention biases, anxiety, and development: toward or away from threats or rewards? Depression and Anxiety 29, 282–294.CrossRefGoogle ScholarPubMed
Strathearn, L (2011). Maternal neglect: oxytocin, dopamine and the neurobiology of attachment. Journal of Neuroendocrinology 23, 1054–1065.CrossRefGoogle ScholarPubMed
Tamietto, M, de Gelder, B (2010). Neural bases of the non-conscious perception of emotional signals. Nature Reviews. Neuroscience 11, 697–709.Google Scholar
Taylor, SE (2006). Tend and befriend: biobehavioral bases of affiliation under stress. Current Directions in Psychological Science 15, 273–277.CrossRefGoogle Scholar
Unkelbach, C, Guastella, AJ, Forgas, JP (2008). Oxytocin selectively facilitates recognition of positive sex and relationship words. Psychological Science 19, 1092–1094.CrossRefGoogle ScholarPubMed
Vuilleumier, P (2005). How brains beware: neural mechanisms of emotional attention. Trends in Cognitive Sciences 9, 585–594.CrossRefGoogle ScholarPubMed
Young, LJ (2009). The neuroendocrinology of the social brain. Frontiers in Neuroendocrinology 30, 425–428.CrossRefGoogle ScholarPubMed