Oxytocin Facilitation of Emotional Empathy Is Associated With Increased Eye Gaze Toward the Faces of Individuals in Emotional Contexts

Jiao Le, Juan Kou, Weihua Zhao, Meina Fu, Yingying Zhang, Benjamin Becker, Keith M Kendrick, Jiao Le, Juan Kou, Weihua Zhao, Meina Fu, Yingying Zhang, Benjamin Becker, Keith M Kendrick

Abstract

One of the most robust effects of intranasal oxytocin treatment is its enhancement of emotional empathy responses across cultures to individuals displaying emotions in realistic contexts in the Multifaceted Empathy Task (MET). However, it is not established if this effect of oxytocin on emotional empathy is due to altered visual attention toward different components of the stimulus pictures or an enhanced empathic response. In the current randomized placebo-controlled within-subject experiment on 40 healthy male individuals, we both attempted a further replication of emotional empathy enhancement by intranasal oxytocin (24 IU) and used eye-tracking measures to determine if this was associated by altered visual attention toward different components of the picture stimuli (background context, human face, and body posture). Results replicated previous findings of enhanced emotional empathy in response to both negative and positive stimuli and that this was associated with an increased proportion of time viewing the faces of humans in the pictures and a corresponding decrease in that toward the rest of the body and/or background context. Overall, our findings suggest that enhanced emotional empathy following oxytocin administration is due to increased attention to the faces of others displaying emotions and away from other contextual and social cues. Clinical Trial Registration: www.ClinicalTrials.gov Oxytocin Modulates Eye Gaze Behavior During Social Processing; registration ID: NCT03293511; URL: https://ichgcp.net/clinical-trials-registry/NCT03293511.

Keywords: autism; emotional empathy; eye gaze; face processing; oxytocin; social attention.

Copyright © 2020 Le, Kou, Zhao, Fu, Zhang, Becker and Kendrick.

Figures

FIGURE 1
FIGURE 1
The effects of oxytocin (OT) on emotional empathy ratings. Subjects were asked to rate positive and negative valence pictures on: “how much do you feel the same as the person in the picture (i.e., direct emotional empathy)” from 1 to 9 (1 = not at all and 9 = very strongly). Error bars represent SEM. **p < 0.01, OXT vs. PLC and positive vs. negative valence.
FIGURE 2
FIGURE 2
The effects of oxytocin (OT) treatment on eye gaze directed toward the face, body, or background regions during the emotional empathy (EE) task. (A) The mean percentage total fixation duration of face, body, and background across two valence (positive, negative). (B) The effects of oxytocin (OT) treatment on mean percentage total fixation duration of face, body, and background across two valence (positive, negative). Error bars represent SEM. ***p < 0.001, *p < 0.05, OXT vs. PLC.
FIGURE 3
FIGURE 3
Correlation (Spearman) between emotional empathy ratings and percentage of total fixation duration using treatment differences scores (i.e., OT minus PLC treatment). Tfd, total fixation duration. Negative face: face region in negative valence pictures. Positive face: face region in positive valence pictures. Emotional empathy ratings for “how much do you feel the same as the person in the picture (i.e., direct emotional empathy)” from 1 to 9 (1 = not at all and 9 = very strongly). OT – PLC, OT minus PLC treatment condition.

References

    1. Abu-Akel A., Palgi S., Klein E., Decety J., Shamay-Tsoory S. (2015). Oxytocin increases empathy to pain when adopting the other- but not self-perspective. Soc. Neurosci. 10 7–15. 10.1080/17470919.2014.948637
    1. 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. Proc. Natl. Acad. Sci. U.S.A. 107 4389–4394. 10.1073/pnas.0910249107
    1. Auyeung B., Lombardo M. V., Heinrichs M., Chakrabarti B., Sule A., Deakin J. B., et al. (2015). Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism. Transl. Psychiatry 5:e507. 10.1038/tp.2014.146
    1. Bernstein D. P., Stein J. A., Newcomb M. D., Walker E., Pogge D., Ahluvalia T., et al. (2003). Development and validation of a brief screening version of the childhood trauma questionnaire. Child Abuse Negl. 27 169–190. 10.1016/S0145-2134(02)00541-0
    1. Chita-Tegmark M. (2016). Social attention in ASD: a review and meta-analysis of eye-tracking studies. Res. Dev. Disabil. 48 79–93. 10.1016/j.ridd.2015.10.011
    1. Davis M. H. (1980). A multidimensional approach to individual differences in empathy. JSAS Catalog Sel. Doc. Psychol. 10 85–103.
    1. Domes G., Heinrichs M., Michel A., Berger C., Herpertz S. C. (2007). Oxytocin improves “mind-reading” in humans. Biol. Psychiatry 61 731–733. 10.1016/j.biopsych.2006.07.015
    1. Domes G., Lischke A., Berger C., Grossmann A., Hauenstein K., Heinrichs M., et al. (2010). Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35 83–93. 10.1016/j.psyneuen.2009.06.016
    1. 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 1198–1202. 10.1016/j.psyneuen.2012.10.002
    1. Dziobek I., Rogers K., Fleck S., Bahnemann M., Heekeren H. R., Wolf O. T., et al. (2008). Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the multifaceted empathy test (MET). J. Autism Dev. Disord. 38 464–473. 10.1007/s10803-007-0486-x
    1. Eckstein M., Bamert V., Stephens S., Wallen K., Young L. J., Ehlert U., et al. (2019). Oxytocin increases eye-gaze towards novel social and non-social stimuli. Soc. Neurosci. 14 594–607. 10.1080/17470919.2018.1542341
    1. Feeser M., Fan Y., Weigand A., Hahn A., Gärtner M., Böker H., et al. (2015). Oxytocin improves mentalizing–pronounced effects for individuals with attenuated ability to empathize. Psychoneuroendocrinology 53 223–232. 10.1016/j.psyneuen.2014.12.015
    1. Gamer M., Zurowski B., Büchel C. (2010). Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc. Natl. Acad. Sci. U.S.A. 107 9400–9405. 10.1073/pnas.1000985107
    1. Gao S., Becker B., Luo L., Geng Y., Zhao W., Yin Y., et al. (2016). Oxytocin, the peptide that bonds the sexes also divides them. Proc. Natl. Acad. Sci. U.S.A. 113 7650–7654. 10.1073/pnas.1602620113
    1. Gau S. S. F., Liu L. T., Wu Y. Y., Chiu Y. N., Tsai W. C. (2013). Psychometric properties of the Chinese version of the social responsiveness scale. Res. Autism Spectr. Disord. 7 349–360. 10.1016/j.rasd.2012.10.004
    1. Geng Y., Zhao W., Zhou F., Ma X., Yao S., Becker B., et al. (2018a). Oxytocin facilitates empathic- and self-embarrassment ratings by attenuating amygdala and anterior insula responses. Front. Endocrinol. 9:572. 10.3389/fendo.2018.00572
    1. Geng Y., Zhao W., Zhou F., Ma X., Yao S., Hurlemann R., et al. (2018b). Oxytocin enhancement of emotional empathy: generalization across cultures and effects on amygdala activity. Front. Neurosci. 12:512. 10.3389/fnins.2018.00512
    1. Guastella A. J., Hickie I. B., McGuinness M. M., Otis M., Woods E. A., Disinger H. M., et al. (2013). Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology 38 612–625. 10.1016/j.psyneuen.2012.11.019
    1. Guastella A. J., Mitchell P. B., Dadds M. R. (2008). Oxytocin increases gaze to the eye region of human faces. Biol. Psychiatry 63 3–5. 10.1016/j.biopsych.2007.06.026
    1. Hubble K., Daughters K., Manstead A. S., Rees A., Thapar A., van Goozen S. H. (2017a). Oxytocin increases attention to the eyes and selectively enhances self-reported affective empathy for fear. Neuropsychologia 106 350–357. 10.1016/j.neuropsychologia.2017.10.019
    1. Hubble K., Daughters K., Manstead A. S., Rees A., Thapar A., van Goozen S. H. (2017b). Oxytocin reduces face processing time but leaves recognition accuracy and eye-gaze unaffected. J. Int. Neuropsychol. Soc. 23 23–33. 10.1017/S1355617716000886
    1. Hurlemann R., Patin A., Onur O. A., Cohen M. X., Baumgartner T., Metzler S., et al. (2010). Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J. Neurosci. 30 4999–5007. 10.1523/JNEUROSCI.5538-09.2010
    1. Kim S., Fonagy P., Koos O., Dorsett K., Strathearn L. (2014). Maternal oxytocin response predicts mother-to-infant gaze. Brain Res. 1580 133–142. 10.1016/j.brainres.2013.10.050
    1. Kou J., Le J., Fu M., Lan C., Chen Z., Li Q., et al. (2019). Comparison of three different eye-tracking tasks for distinguishing autistic from typically developing children and autistic symptom severity. Autism Res. 12 1529–1540. 10.1002/aur.2174
    1. Lau W. Y. P., Gau S. S. F., Chiu Y. N., Wu Y. Y., Chou W. J., Liu S. K., et al. (2013). Psychometric properties of the Chinese version of the Autism Spectrum Quotient (AQ). Res. Dev. Disabil. 34 294–305. 10.1016/j.ridd.2012.08.005
    1. Le J., Kou J., Zhao W., Fu M., Zhang Y., Becker B., et al. (2020). Oxytocin biases eye-gaze to dynamic and static social images and the eyes of fearful faces: associations with trait autism. Trans Psychiatry 10:142. 10.1038/s41398-020-0830-x
    1. Lieberz J., Scheele D., Spengler F. B., Mathiesen T., Schneider L., Stoffel-Wagner B., et al. (2019). Kinetics of oxytocin effects on amygdala and striatal reactivity vary between women and men. Neuropsychopharmacology 45 1134–1140. 10.1038/s41386-019-0582-6
    1. 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 37 475–481. 10.1016/j.psyneuen.2011.07.015
    1. Lischke A., Herpertz S. C., Berger C., Domes G., Gamer M. (2017). Divergent effects of oxytocin on (para-) limbic reactivity to emotional and neutral scenes in females with and without borderline personality disorder. Soc. Cogn. Affect. Neurosci. 12 1783–1792. 10.1093/scan/nsx107
    1. Lombardo M. V., Barnes J. L., Wheelwright S. J., Baron-Cohen S. (2007). Self-referential cognition and empathy in autism. PLoS One 2:e883. 10.1371/journal.pone.0000883
    1. Luo L., Becker B., Geng Y., Zhao Z., Gao S., Zhao W., et al. (2017). Sex-dependent neural effect of oxytocin during subliminal processing of negative emotion faces. Neuroimage 162 127–137. 10.1016/j.neuroimage.2017.08.079
    1. Nishizato M., Fujisawa T. X., Kosaka H., Tomoda A. (2017). Developmental changes in social attention and oxytocin levels in infants and children. Sci. Rep. 7:2540. 10.1038/s41598-017-02368-x
    1. Radke S., de Bruijn E. R. A. (2015). Does oxytocin affect mind-reading? A replication study. Psychoneuroendocrinology 60 75–81. 10.1016/j.psyneuen.2015.06.006
    1. Riem M. M. E., 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. Prog. Neuropsychopharmacol Biol. Psychiatry 51 105–112. 10.1016/j.pnpbp.2014.01.014
    1. 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 1929–1936. 10.1038/npp.2013.86
    1. Shamay-Tsoory S. G., Abu-Akel A., Palgi S., Sulieman R., Fischer-Shofty M., Levkovitz Y., et al. (2013). Giving peace a chance: oxytocin increases empathy to pain in the context of the Israeli-Palestinian conflict. Psychoneuroendocrinology 38 3139–3144. 10.1016/j.psyneuen.2013.09.015
    1. Shamay-Tsoory S. G. (2011). The neural bases for empathy. Neuroscientist 17 18–24. 10.1177/1073858410379268
    1. Shamay-Tsoory S. G., Abu-Akel A. (2016). The social salience hypothesis of oxytocin. Biol. Psychiatry 79 194–202. 10.1016/j.biopsych.2015.07.020
    1. Shek D. T. (1993). The Chinese version of the state-trait anxiety inventory: its relationship to different measures of psychological well-being. J. Clin. Psychol. 49 349–358. 10.1002/1097-4679(199305)49:3<349::AID-JCLP2270490308>;2-J
    1. Tully E. C., Ames A. M., Garcia S. E., Donohue M. R. (2016). Quadratic Associations between empathy and depression as moderated by emotion dysregulation. J. Psychol. 150 15–35. 10.1080/00223980.2014.992382
    1. Watson D., Clark L. A., Tellegen A. (1988). Development and validation of brief measures of positive and negative affect: the PANAS scales. J. Pers. Soc. Psychol. 54 1063–1070. 10.1037/0022-3514.54.6.1063
    1. Xu L., Ma X., Zhao W., Luo L., Yao S., Kendrick K. M. (2015). Oxytocin enhances attentional bias for neutral and positive expression faces in individuals with higher autistic traits. Psychoneuroendocrinology 62 352–358. 10.1016/j.psyneuen.2015.09.002
    1. Xu X., Dai J., Liu C., Chen Y., Xin F., Zhou F., et al. (2020). Common and disorder-specific neurofunctional markers of dysregulated empathic reactivity in major depression and generalized anxiety disorder. Psychotherapy and Psychosomatics 89 114–116. 10.1159/000504180
    1. Xu X., Li J., Chen Z., Kendrick K. M., Becker B. (2019). Oxytocin reduces top-down control of attention by increasing bottom-up attention allocation to social but not non-social stimuli–a randomized controlled trial. Psychoneuroendocrinology 108 62–69. 10.1016/j.psyneuen.2019.06.004
    1. Yao S., Becker B., Zhao W., Zhao Z., Kou J., Ma X., et al. (2018). Oxytocin modulates attention switching between interoceptive signals and external social cues. Neuropsychopharmacology 43 294–301. 10.1038/npp.2017.189
    1. Zhao X., Zhang Y., Longfei L. I., Zhou Y. (2005). Evaluation on reliability and validity of Chinese version of childhood trauma questionnaire. Chinese J. Tissue Eng. Res. 9 209–211.

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