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Oxytocin Reduces Face Processing Time but Leaves Recognition Accuracy and Eye-Gaze Unaffected

Published online by Cambridge University Press:  21 November 2016

Kelly Hubble
Affiliation:
School of Psychology, Cardiff University, Cardiff, United Kingdom
Katie Daughters
Affiliation:
School of Psychology, Cardiff University, Cardiff, United Kingdom
Antony S.R. Manstead
Affiliation:
School of Psychology, Cardiff University, Cardiff, United Kingdom
Aled Rees
Affiliation:
Institute of Molecular and Experimental Medicine, School of Medicine, Cardiff University, Cardiff, United Kingdom
Anita Thapar
Affiliation:
Institute of Psychological Medicine and Clinical Neurosciences, School of Medicine, Cardiff University, Cardiff, United Kingdom
Stephanie H.M. van Goozen*
Affiliation:
School of Psychology, Cardiff University, Cardiff, United Kingdom
*
Correspondence and reprint requests to: Stephanie van Goozen, School of Psychology, Cardiff University, Tower Building, 70 Park Place, Cardiff, CF10 3AT. E-mail: vangoozens@cardiff.ac.uk

Abstract

Objectives: Previous studies have found that oxytocin (OXT) can improve the recognition of emotional facial expressions; it has been proposed that this effect is mediated by an increase in attention to the eye-region of faces. Nevertheless, evidence in support of this claim is inconsistent, and few studies have directly tested the effect of oxytocin on emotion recognition via altered eye-gaze Methods: In a double-blind, within-subjects, randomized control experiment, 40 healthy male participants received 24 IU intranasal OXT and placebo in two identical experimental sessions separated by a 2-week interval. Visual attention to the eye-region was assessed on both occasions while participants completed a static facial emotion recognition task using medium intensity facial expressions. Results: Although OXT had no effect on emotion recognition accuracy, recognition performance was improved because face processing was faster across emotions under the influence of OXT. This effect was marginally significant (p<.06). Consistent with a previous study using dynamic stimuli, OXT had no effect on eye-gaze patterns when viewing static emotional faces and this was not related to recognition accuracy or face processing time. Conclusions: These findings suggest that OXT-induced enhanced facial emotion recognition is not necessarily mediated by an increase in attention to the eye-region of faces, as previously assumed. We discuss several methodological issues which may explain discrepant findings and suggest the effect of OXT on visual attention may differ depending on task requirements. (JINS, 2017, 23, 23–33)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2016 

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References

Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience, 14(8), 12641274.CrossRefGoogle ScholarPubMed
Andari, E., Duhamel, J.R., Zalla, T., Herbrecht, E., Leboyer, M., & Sirigu, A. (2010). Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proceeding of the National Academy of Sciences of the United States of America, 107(9), 43894394. doi: 10.1073/pnas.0910249107 CrossRefGoogle ScholarPubMed
Bartz, J.A., Zaki, J., Bolger, N., Hollander, E., Ludwig, N.N., Kolevzon, A. & Ochsner, K.N. (2010). Oxytocin selectively improves empathic accuracy. Psychological Science, 21(10), 14261428. doi: 10.1177/0956797610383439.CrossRefGoogle ScholarPubMed
Beery, A.K. (2015). Antisocial oxytocin: Complex effects on social behavior. Current Opinion in Behavioral Sciences, 6, 174182. doi: 10.1016/j.cobeha.2015.11.006 CrossRefGoogle Scholar
Bowen, K.L., Morgan, J.E., Moore, S.C., & Van Goozen, S.H.M. (2014). Young offenders’ emotion recognition dysfunction across emotion intensities: Explaining variation using psychopathic traits, conduct disorder and offense severity. Journal of Psychopathology and Behaviour Assessment, 36(1), 6073. doi: 10.1007/s10862-013-9368-z CrossRefGoogle ScholarPubMed
Bradley, M.M., Miccoli, L., Escrig, M.A., & Lang, P.J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45(4), 602607. doi: 10.1111/j.1469-8986.2008.00654.x CrossRefGoogle ScholarPubMed
Carr, M.B., & Lutjemeier, J. A. (2005). The relation of facial affect recognition and empathy to delinquency in youth offenders. Adolescence, 40(159), 601619.Google ScholarPubMed
Churchland, P.S., & Winkielman, P. (2012). Modulating social behavior with oxytocin: How does it work? What does it mean? Hormones & Behavior, 61, 392399. doi: 10.1016/j.yhbeh.2011.12.003 CrossRefGoogle ScholarPubMed
Daughters, K., Manstead, A.S.R., Hubble, K., Rees, A., Thapar, A., & van Goozen, S. H. M. (2015). Salivary oxytocin concentrations in males following intranasal administration of oxytocin: A double-blind, cross-over study. PloS One, 10(12), e0145104. doi: 10.1371/journal.pone.0145104 CrossRefGoogle ScholarPubMed
DeWall, C.N., Gillath, O., Pressman, S.D., Black, L.L., Bartz, J.A., Moskovitz, J., & Stetler, D.A. (2014). When the love hormone leads to violence: Oxytocin increases intimate partner violence inclinations among high trait aggressive people. Social Psychological and Personality Science, 5(6), 691697. doi: 10.1177/1948550613516876 CrossRefGoogle Scholar
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S.C. (2007). Oxytocin improves “mind-reading” in humans. Biological Psychiatry, 61(6), 731733.CrossRefGoogle ScholarPubMed
Domes, G., Lischke, A., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., & Herpertz, S.C. (2010). Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology, 35(1), 8393. doi: 10.1016/j.psyneuen.2009.06.016 CrossRefGoogle ScholarPubMed
Domes, G., Steiner, A., Porges, S.W., & Heinrichs, M. (2013). Oxytocin differentially modulates eye gaze to naturalistic social signals of happiness and anger. Psychoneuroendocrinology, 38(7), 11981202. doi: 10.1016/j.psyneuen.2012.10.002 CrossRefGoogle ScholarPubMed
Ekman, P., & Friesen, W.V. (1975). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Fischer-Shofty, M., Shamay-Tsoory, S.G., Harari, H., & Levkovitz, Y. (2010). The effect of intranasal administration of oxytocin on fear recognition. Neuropsychologia, 48(1), 179184. doi: 10.1016/j.neuropsychologia.2009.09.003 CrossRefGoogle ScholarPubMed
Fox, E., Lester, V., Russo, R., Bowles, R.J., Pichler, A., & Dutton, K. (2000). Facial expressions of emotion: Are angry faces detected more efficiently? Cognition and Emotion, 14(1), 6192. doi: 10.1080/026999300378996 CrossRefGoogle ScholarPubMed
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 of the United States of America, 107(20), 94009405. doi: 10.1073/pnas.1000985107 CrossRefGoogle ScholarPubMed
Guastella, A.J., Mitchell, P.B., & Dadds, M.R. (2008). Oxytocin increases gaze to the eye region of human faces. Biological Psychiatry, 63(1), 35.CrossRefGoogle Scholar
Heinrichs, M., von Dawans, B., & Domes, G. (2009). Oxytocin, vasopressin, and human social behavior. Frontiers in Neuroendocrinology, 30(4), 548557. doi: 10.1016/j.yfrne.2009.05.005 CrossRefGoogle ScholarPubMed
Hoffmann, H., Kessler, H., Eppel, T., Rukavina, S., & Traue, H.C. (2010). Expression intensity, gender and facial emotion recognition: Women recognize only subtle facial emotions better than men. Acta Psychologica, 135(3), 278283. doi: 10.1016/j.actpsy.2010.07.012 CrossRefGoogle ScholarPubMed
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. Journal of Neuroscience, 25(49), 1148911493. doi: 10.1523/JNEUROSCI.3984-05.2005 CrossRefGoogle ScholarPubMed
Kosfeld, M., Heinrichs, M., Zak, P.J., Fischbacher, U., & Fehr, E. (2005). Oxytocin increases trust in humans. Nature, 435, 673676. doi: 10.1038/nature03701 CrossRefGoogle ScholarPubMed
Leknes, S., Wessberg, J., Ellingsen, D.-M., Chelnokova, O., Olausson, H., & Laeng, B. (2012). Oxytocin enhances pupil dilation and sensitivity to “hidden” emotional expressions. Social Cognitive and Affective Neuroscience, 8, 741749. doi: 10.1093/scan/nss062 CrossRefGoogle ScholarPubMed
Leng, G., & Ludwig, M. (2016). Intranasal oxytocin: Myths and delusions. Biological Psychiatry, 79(3), 243250. doi: 10.1016/j.biopsych.2015.05.003 CrossRefGoogle ScholarPubMed
Leppänen, J.M., & Hietanen, J.K. (2004). Positive facial expressions are recognized faster than negative facial expressions, but why? Psychological Research, 69, 2229.CrossRefGoogle ScholarPubMed
Lischke, A., Berger, C., Prehn, K., Heinrichs, M., Herpertz, S.C., & Domes, G. (2012). Intranasal oxytocin enhances emotion recognition from dynamic facial expressions and leaves eye-gaze unaffected. Psychoneuroendocrinology, 37(4), 475481. doi: 10.1016/j.psyneuen.2011.07.015 CrossRefGoogle ScholarPubMed
Lischke, A., Gamer, M., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., & Domes, G. (2012). Oxytocin increases amygdala reactivity to threatening scenes in females. Psychoneuroendocrinology, 37(9), 14311438. doi: 10.1016/j.psyneuen.2012.01.011 CrossRefGoogle ScholarPubMed
Marsh, A.A., Yu, H.H., Pine, D.S., & Blair, R.J.R. (2010). Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology, 209(3), 225332. doi: 10.1007/s00213-010-1780-4 CrossRefGoogle ScholarPubMed
Prehn, K., Kazzer, P., Lischke, A., Heinrichs, M., Herpertz, S.C., & Domes, G. (2013). Effects of intranasal oxytocin on pupil dilation indicate increased salience of socioaffective stimuli. Psychophysiology, 50(6), 528537. doi: 10.1111/psyp.12042 CrossRefGoogle ScholarPubMed
Rieger, G., & Savin-Williams, R.C. (2012). The eyes have it: Sex and sexual orientation differences in pupil dilation patterns. PLoS One, 7(8), e40256. doi: 10.1371/journal.pone.0040256 CrossRefGoogle ScholarPubMed
Shahrestani, S., Kemp, A.H., & Guastella, A. J. (2013). The impact of a single administration of intranasal oxytocin on the recognition of basic emotions in humans: A meta-analysis. Neuropsychopharmacology, 38(10), 19291936. doi: 10.1038/npp.2013.86 CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S.G., Fischer, M., Dvash, J., Harari, H., Perach-Bloom, N., & Levkovitz, Y. (2009). Intranasal administration of oxytocin increases envy and schadenfreude (gloating). Biological Psychiatry, 66(9), 864887. doi: 10.1016/j.biopsych.2009.06.009 CrossRefGoogle ScholarPubMed
Schnys, P.G., Petro, L., & Smith, M.L. (2009). Transmission of facial expressions of emotion co-evolved with their efficient decoding in the brain: Behavioral and brain evidence. PLoS One, 4(5), e5625. doi: 10.1371/journal.pone.0005625 CrossRefGoogle Scholar
Theodoridou, A., Rowe, A.C., Penton-Voak, I.S., & Rogers, P.J. (2009). Oxytocin and social perception: Oxytocin increases perceived facial trustworthiness and attractiveness. Hormones and Behavior, 56(1), 128132. doi: 10.1016/j.yhbeh.2009.03.019 CrossRefGoogle ScholarPubMed
Valla, J.M., Maendel, J.W., Ganzel, B.L., Barsky, A.R., & Belmonte, M.K. (2013). Autistic trait interactions underlie sex-dependent facial recognition abilities in the normal population. Frontiers in Psychology, 4, 286. doi: 10.3389/fpsyg.2013.00286 CrossRefGoogle ScholarPubMed
Vo, M.L.H., Smith, T.J., Mital, P.K., & Henderson, J.M. (2012). Do the eyes really have it? Dynamic allocation of attention when viewing moving faces. Journal of Vision, 12(13), 114. doi: 10.1167/12.13.3 CrossRefGoogle ScholarPubMed
Walum, H., Waldman, I.D., & Young, L.J. (2016). Statistical and methodological considerations for the interpretation of intranasal oxytocin studies. Biological Psychiatry, 79(3), 251257. doi: 10.1016/j.biopsych.2015.06.016 CrossRefGoogle ScholarPubMed
Zak, P.J., Stanton, A.A., & Ahmadi, S. (2007). Oxytocin increases generosity in humans. PLoS One, 2(11), e1128.CrossRefGoogle ScholarPubMed