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The role of oxytocin in empathy to the pain of conflictual out-group members among patients with schizophrenia

Published online by Cambridge University Press:  24 April 2014

A. Abu-Akel ,
M. Fischer-Shofty ,
Y. Levkovitz ,
J. Decety  and
S. Shamay-Tsoory
A. Abu-Akel*
Affiliation:
School of Psychology, University of Birmingham, UK
M. Fischer-Shofty
Affiliation:
Department of Psychology, University of Haifa, Israel
Y. Levkovitz
Affiliation:
The Emotion-Cognition Research Center, Shalvata Mental Health Care Center, Hod-Hasharon, Israel
J. Decety
Affiliation:
Department of Psychology, University of Chicago, USA
S. Shamay-Tsoory
Affiliation:
Department of Psychology, University of Haifa, Israel
*
*Address for correspondence: A. Abu-Akel, School of Psychology, University of Birmingham, Birmingham B15 2TT, UK. (Email: ama289@bham.ac.uk)
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Abstract

Background.

Oxytocin (OT) is associated with our ability to empathize and has been shown to play a major role in mediating social behaviors within the context of intergroup dynamics. Schizophrenia is associated with impaired empathy, and with a dysfunctional oxytocinergic system. The effect of OT on the empathic responses of patients with schizophrenia within the context of intergroup relationships has not been studied. The present study examined the effect of OT on the patients' empathic responses to pain experienced by in-group, conflictual out-group and neutral out-group members.

Method.

In a double-blind, placebo-controlled, within-subject cross-over design, the responses on the Pain Evaluation Task of 28 male patients with schizophrenia were compared to 27 healthy male controls. All participants received a single intranasal dose of 24 IU OT or placebo, 1 week apart.

Results.

OT induced an empathy bias in the healthy controls towards the conflictual out-group members. Although this effect was absent in the patient group, OT seems to heighten an empathic bias in the patient group towards the in-group members when rating non-painful stimuli.

Conclusions.

The study demonstrates that the administration of OT can result in empathic bias towards adversary out-group members in healthy controls but not in patients with schizophrenia. However, the OT-induced bias in both the patients (in the no-pain condition towards the in-group members) and the healthy controls (in the no-pain and pain conditions towards the adversary out-group) suggests that OT enhances the distinction between conflictual in-group and out-group members.

Keywords

Empathyintergroup dynamicsoxytocinpainschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 16 , December 2014 , pp. 3523 - 3532
Copyright
Copyright © Cambridge University Press 2014 

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References

Abu-Akel, A (2008). Theory of mind in autism, schizophrenia, and in-between. Behavioral and Brain Sciences 31, 261–262.Google Scholar
Abu-Akel, A, Abushua'leh, K (2004). ‘Theory of mind’ in violent and nonviolent patients with paranoid schizophrenia. Schizophrenia Research 69, 45–53.CrossRefGoogle ScholarPubMed
Abu-Akel, A, Bailey, AL (2000). The possibility of different forms of theory of mind impairment in psychiatric and developmental disorders. Psychological Medicine 30, 735–738.Google Scholar
Abu-Akel, A, Bo, H (2013). Superior mentalizing abilities of female patients with schizophrenia. Psychiatry Research 210, 794–799.Google Scholar
Akitsuki, Y, Decety, J (2009). Social context and perceived agency affects empathy for pain: an event-related fMRI investigation. NeuroImage 47, 722–734.Google Scholar
Averbeck, BB, Bobin, T, Evans, S, Shergill, SS (2012). Emotion recognition and oxytocin in patients with schizophrenia. Psychological Medicine 42, 259–266.Google Scholar
Baron-Cohen, S, Wheelwright, S (2004). The Empathy Quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders 34, 163–175.Google Scholar
Bartz, JA, Zaki, J, Bolger, N, Ochsner, KN (2011). Social effects of oxytocin in humans: context and person matter. Trends in Cognitive Sciences 15, 301–309.Google Scholar
Batson, CD, Early, S, Salvarani, G (1987). Perspective taking: imagining how another feels versus imaging how you would feel. Personality and Social Psychology Bulletin 23, 751–758.Google Scholar
Beckmann, H, Lang, RE, Gattaz, WF (1985). Vasopressin–oxytocin in cerebrospinal fluid of schizophrenic patients and normal controls. Psychoneuroendocrinology 10, 187–191.Google Scholar
Bethlehem, RA, van Honk, J, Auyeung, B, Baron-Cohen, S (2013). Oxytocin, brain physiology, and functional connectivity: a review of intranasal oxytocin fMRI studies. Psychoneuroendocrinology 38, 962–974.Google Scholar
Blair, RJR (2005). Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations. Consciousness and Cognition 15, 698–718.Google Scholar
Bora, E, Gokcen, S, Veznedaroglu, B (2008). Empathic abilities in people with schizophrenia. Psychiatry Research 160, 23–29.Google Scholar
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
Bruneau, EG, Dufour, N, Saxe, R (2012). Social cognition in members of conflict groups: behavioural and neural responses in Arabs, Israelis and South Americans to each other's misfortunes. Philosophical Transactions of the Royal Society. Series B, Biological Sciences 367, 717–730.Google Scholar
Bujanow, W (1974). Letter: Is oxytocin an anti-schizophrenic hormone? Canadian Journal of Psychiatry 19, 323.Google Scholar
Caldwell, HK, Stephens, SL, Young, WS 3rd (2009). Oxytocin as a natural antipsychotic: a study using oxytocin knockout mice. Molecular Psychiatry 14, 190–196.CrossRefGoogle ScholarPubMed
Davis, MC, Lee, J, Horan, WP, Clarke, AD, McGee, MR, Green, MF, Marder, SR (2013). Effects of single dose intranasal oxytocin on social cognition in schizophrenia. Schizophrenia Research 147, 393–397.Google Scholar
Decety, J, Echols, S, Correll, J (2010). The blame game: the effect of responsibility and social stigma on empathy for pain. Journal of Cognitive Neuroscience 22, 985–997.Google Scholar
Decety, J, Lamm, C (2006). Human empathy through the lens of social neuroscience. Scientific World Journal 6, 1146–1163.Google Scholar
Decety, J, Svetlova, M (2012). Putting together phylogenetic and ontogenetic perspectives on empathy. Developmental Cognitive Neuroscience 2, 1–24.Google Scholar
De Dreu, CK (2012). Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda. Hormones and Behavior 61, 419–428.Google Scholar
De Dreu, CK, Greer, LL, Handgraaf, MJ, Shalvi, S, Van Kleef, GA, Baas, M, Ten Velden, FS, Van Dijk, E, Feith, SW (2010). The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 328, 1408–1411.CrossRefGoogle ScholarPubMed
De Dreu, CK, Greer, LL, Van Kleef, GA, Shalvi, S, Handgraaf, MJ (2011). Oxytocin promotes human ethnocentrism. Proceedings of the National Academy of Sciences USA 108, 1262–1266.Google Scholar
Derntl, B, Finkelmeyer, A, Toygar, TK, Hulsmann, A, Schneider, F, Falkenberg, DI, Habel, U (2009). Generalized deficit in all core components of empathy in schizophrenia. Schizophrenia Research 108, 197–206.CrossRefGoogle ScholarPubMed
Feifel, D, Macdonald, K, Cobb, P, Minassian, A (2012). Adjunctive intranasal oxytocin improves verbal memory in people with schizophrenia. Schizophrenia Research 139, 207–210.Google Scholar
Feifel, D, Macdonald, K, Nguyen, A, Cobb, P, Warlan, H, Galangue, B, Minassian, A, Becker, O, Cooper, J, Perry, W, Lefebvre, M, Gonzales, J, Hadley, A (2010). Adjunctive intranasal oxytocin reduces symptoms in schizophrenia patients. Biological Psychiatry 68, 678–680.Google Scholar
Fischer-Shofty, M, Brune, M, Ebert, A, Shefet, D, Levkovitz, Y, Shamay-Tsoory, SG (2013). Improving social perception in schizophrenia: the role of oxytocin. Schizophrenia Research 146, 357–362.Google Scholar
Frith, CD (2004). Schizophrenia and theory of mind. Psychological Medicine 34, 385–389.CrossRefGoogle ScholarPubMed
Goldman, M, Marlow-O'Connor, M, Torres, I, Carter, CS (2008). Diminished plasma oxytocin in schizophrenic patients with neuroendocrine dysfunction and emotional deficits. Schizophrenia Research 98, 247–255.Google Scholar
Gossen, A, Hahn, A, Westphal, L, Prinz, S, Schultz, RT, Grunder, G, Spreckelmeyer, KN (2012). Oxytocin plasma concentrations after single intranasal oxytocin administration – a study in healthy men. Neuropeptides 46, 211–215.Google Scholar
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.Google Scholar
Hayes, DJ, Northoff, G (2012). Common brain activations for painful and non-painful aversive stimuli. BMC Neuroscience 13, 60.CrossRefGoogle ScholarPubMed
Hein, G, Silani, G, Preuschoff, K, Batson, CD, Singer, T (2010). Neural responses to ingroup and outgroup members’ suffering predict individual differences in costly helping. Neuron 68, 149–160.CrossRefGoogle ScholarPubMed
Hurlemann, R, Patin, A, Onur, OA, Cohen, MX, Baumgartner, T, Metzler, S, Dziobek, I, Gallinat, J, Wagner, M, Maier, W, Kendrick, KM (2010). Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. Journal of Neuroscience 30, 4999–5007.Google Scholar
Jackson, PL, Decety, J (2004). Motor cognition: a new paradigm to study self-other interactions. Current Opinion in Neurobiology 14, 259–263.CrossRefGoogle ScholarPubMed
Jackson, PL, Meltzoff, AN, Decety, J (2005). How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage 24, 771–779.Google Scholar
Juif, PE, Poisbeau, P (2013). Neurohormonal effects of oxytocin and vasopressin receptor agonists on spinal pain processing in male rats. Pain 154, 1449–1456.Google Scholar
Kapur, S (2003). Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry 160, 3–23.Google Scholar
Kavaliers, M, Choleris, E (2011). Sociality, pathogen avoidance, and the neuropeptides oxytocin and arginine vasopressin. Psychological Science 22, 1367–1374.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.Google Scholar
Kemp, AH, Guastella, AJ (2011). The role of oxytocin in human affect: a novel hypothesis. Current Directions in Psychological Science 20, 222–231.CrossRefGoogle Scholar
Keri, S, Kiss, I, Kelemen, O (2009). Sharing secrets: oxytocin and trust in schizophrenia. Social Neuroscience 4, 287–293.Google Scholar
Komorita, SS, Parks, CD (1995). Interpersonal relations: mixed-motive interaction. Annual Review of Psychology 46, 183–207.CrossRefGoogle Scholar
Lee, J, Zaki, J, Harvey, PO, Ochsner, K, Green, MF (2011). Schizophrenia patients are impaired in empathic accuracy. Psychological Medicine 41, 2297–2304.Google Scholar
Legros, JJ, Gazzotti, C, Carvelli, T, Franchimont, P, Timsit-Berthier, M, von Frenckell, R, Ansseau, M (1992). Apomorphine stimulation of vasopressin- and oxytocin-neurophysins. Evidence for increased oxytocinergic and decreased vasopressinergic function in schizophrenics. Psychoneuroendocrinology 17, 611–617.Google Scholar
Leknes, S, Wessberg, J, Ellingsen, DM, Chelnokova, O, Olausson, H, Laeng, B (2013). Oxytocin enhances pupil dilation and sensitivity to ‘hidden’ emotional expressions. Social Cognitive and Affective Neuroscience 8, 741–749.CrossRefGoogle ScholarPubMed
Linkowski, P, Geenen, V, Kerkhofs, M, Mendlewicz, J, Legros, JJ (1984). Cerebrospinal fluid neurophysins in affective illness and in schizophrenia. European Archive of Psychiatry and Clinical Neuroscience 234, 162–165.Google Scholar
McCarthy, MM (1995). Estrogen modulation of oxytocin and its relation to behavior. Advances in Experimental Medicine and Biology 395, 235–245.Google Scholar
Montag, C, Brockmann, EM, Bayerl, M, Rujescu, D, Muller, DJ, Gallinat, J (2012 a). Oxytocin and oxytocin receptor gene polymorphisms and risk for schizophrenia: a case-control study. World Journal of Biological Psychiatry 14, 500–508.Google Scholar
Montag, C, Brockmann, EM, Lehmann, A, Muller, DJ, Rujescu, D, Gallinat, J (2012 b). Association between oxytocin receptor gene polymorphisms and self-rated ‘empathic concern’ in schizophrenia. PLoS One 7, e51882.Google Scholar
Montag, C, Dziobek, I, Richter, IS, Neuhaus, K, Lehmann, A, Sylla, R, Heekeren, HR, Heinz, A, Gallinat, J (2011). Different aspects of theory of mind in paranoid schizophrenia: evidence from a video-based assessment. Psychiatry Research 186, 203–209.Google Scholar
Mouraux, A, Diukova, A, Lee, MC, Wise, RG, Iannetti, GD (2011). A multisensory investigation of the functional significance of the ‘pain matrix’. NeuroImage 54, 2237–2249.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
Petrovic, P, Kalisch, R, Singer, T, Dolan, RJ (2008). Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. Journal of Neuroscience 28, 6607–6615.CrossRefGoogle ScholarPubMed
Rosenfeld, AJ, Lieberman, JA, Jarskog, LF (2011). Oxytocin, dopamine, and the amygdala: a neurofunctional model of social cognitive deficits in schizophrenia. Schizophrenia Bulletin 37, 1077–1087.CrossRefGoogle ScholarPubMed
Rubin, LH, Carter, CS, Drogos, L, Pournajafi-Nazarloo, H, Sweeney, JA, Maki, PM (2010). Peripheral oxytocin is associated with reduced symptom severity in schizophrenia. Schizophrenia Research 124, 13–21.Google Scholar
Sasayama, D, Hattori, K, Teraishi, T, Hori, H, Ota, M, Yoshida, S, Arima, K, Higuchi, T, Amano, N, Kunugi, H (2012). Negative correlation between cerebrospinal fluid oxytocin levels and negative symptoms of male patients with schizophrenia. Schizophrenia Research 139, 201–206.Google Scholar
Shamay-Tsoory, SG (2011). The neural bases for empathy. Neuroscientist 17, 18–24.Google Scholar
Shamay-Tsoory, SG, Abu-Akel, A, Palgi, S, Sulieman, R, Fischer-Shofty, M, Levkovitz, Y, Decety, J (2013). Giving peace a chance: oxytocin increases empathy to pain in the context of the Israeli-Palestinian conflict. Psychoneuroendocrinology 38, 3139–3144.Google Scholar
Shipley, WC (1940). A self-administering scale for measuring intellectual impairment and deterioration. Journal of Psychology 9, 371–377.Google Scholar
Singer, T, Seymour, B, O'Doherty, J, Kaube, H, Dolan, RJ, Frith, CD (2004). Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1162.Google Scholar
Smith, MJ, Horan, WP, Cobia, DJ, Karpouzian, TM, Fox, JM, Reilly, JL, Breiter, HC (2013). Performance-based empathy mediates the influence of working memory on social competence in schizophrenia. Schizophrenia Bulletin. Published online: 31 December 2013 . doi: 10.1093/schbul/sbt084.Google ScholarPubMed
Souza, RP, Ismail, P, Meltzer, HY, Kennedy, JL (2010). Variants in the oxytocin gene and risk for schizophrenia. Schizophrenia Research 121, 279–280.Google Scholar
Striepens, N, Kendrick, KM, Maier, W, Hurlemann, R (2011). Prosocial effects of oxytocin and clinical evidence for its therapeutic potential. Frontiers in Neuroendocrinology 32, 426–450.Google Scholar
Tarrant, M, Dazeley, S, Cottom, T (2009). Social categorization and empathy for outgroup members. British Journal of Social Psychology 48, 427–446.Google Scholar
Trawalter, S, Hoffman, KM, Waytz, A (2012). Racial bias in perceptions of others’ pain. PLoS One 7, e48546.Google Scholar
Walss-Bass, C, Fernandes, JM, Roberts, DL, Service, H, Velligan, D (2013). Differential correlations between plasma oxytocin and social cognitive capacity and bias in schizophrenia. Schizophrenia Research 147, 387–392.Google Scholar