Oxytocin biases men but not women to restore social connections with individuals who socially exclude them

We normally react to individuals who exclude us socially by either avoiding them or increasing our attempts to interact with them. The neuropeptide oxytocin can promote social bonds and reduce social conflict and we therefore investigated whether it facilitates more positive social responses towards individuals who exclude or include us. In a double-blind, placebo-controlled, between-subject design 77 healthy Chinese male and female participants received intranasal oxytocin (40 IU) or placebo before playing a modified virtual ball-tossing game with three fictitious partners who either showed exclusion, inclusion or neutral behavioral interactions with them. Results showed that both male and female subjects threw the ball more often to individuals who excluded rather than included them, although oxytocin did not alter this or awareness/feelings of exclusion or inclusion. However, when subjects returned a week later males, but not females, in the oxytocin group exhibited an increased liking for, and preference for playing again with, players who had previously excluded them. This oxytocin effect was positively associated with independent traits. Our findings suggest that in a collectivist culture oxytocin may promote the desire of males, but not females, with a stronger independent orientation to rebuild social connections with individuals who have previously excluded them.

[1]  John Ewer,et al.  Oxytocin and Vasopressin Receptor Gene Polymorphisms: Role in Social and Psychiatric Traits , 2016, Front. Neurosci..

[2]  Rick Richardson,et al.  How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence , 2004 .

[3]  K. Trzesniewski,et al.  Measuring Global Self-Esteem: Construct Validation of a Single-Item Measure and the Rosenberg Self-Esteem Scale , 2001 .

[4]  G. Leng,et al.  Intranasal Oxytocin: Myths and Delusions , 2016, Biological Psychiatry.

[5]  G. Echterhoff,et al.  The interplay of oxytocin and collectivistic orientation shields against negative effects of ostracism , 2014 .

[6]  Shiwei Jia,et al.  Are we sensitive to valence differences in emotionally negative stimuli? Electrophysiological evidence from an ERP study , 2007, Neuropsychologia.

[7]  Steve W. C. Chang,et al.  Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta) , 2012, Proceedings of the National Academy of Sciences.

[8]  L. Hanson,et al.  Novel Vasoconstrictor Formulation to Enhance Intranasal Targeting of Neuropeptide Therapeutics to the Central Nervous System , 2009, Journal of Pharmacology and Experimental Therapeutics.

[9]  M. Gelfand,et al.  Horizontal and Vertical Dimensions of Individualism and Collectivism: A Theoretical and Measurement Refinement , 1995 .

[10]  K. Jonas,et al.  Out of the group, out of control? The brain responds to social exclusion with changes in cognitive control. , 2013, Social cognitive and affective neuroscience.

[11]  K. Macdonald,et al.  Oxytocin׳s role in anxiety: A critical appraisal , 2014, Brain Research.

[12]  L. Parr,et al.  Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques , 2014, Psychoneuroendocrinology.

[13]  Kipling D. Williams,et al.  Chapter 6 Ostracism: A Temporal Need‐Threat Model , 2009 .

[14]  P. Falkai,et al.  Effects of social exclusion on emotions and oxytocin and cortisol levels in patients with chronic depression. , 2015, Journal of psychiatric research.

[15]  C. Grillon,et al.  Oxytocin increases anxiety to unpredictable threat , 2013, Molecular Psychiatry.

[16]  K. Bales,et al.  Plasma and CSF oxytocin levels after intranasal and intravenous oxytocin in awake macaques , 2016, Psychoneuroendocrinology.

[17]  J. Cacioppo,et al.  Negative information weighs more heavily on the brain: The negativity bias in evaluative categorizations. , 1998 .

[18]  Markus Heinrichs,et al.  Oxytocin and the social brain: Neural mechanisms and perspectives in human research , 2014, Brain Research.

[19]  K. Kendrick,et al.  Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans , 2013, Scientific Reports.

[20]  M. Pillutla,et al.  Social reconnection revisited: The effects of social exclusion risk on reciprocity, trust, and general risk-taking , 2010 .

[21]  W. S. Applied Psychology , 1926, Nature.

[22]  Michael J. Bernstein,et al.  Adaptive Responses to Social Exclusion , 2008, Psychological science.

[23]  Matthew D. Lieberman,et al.  Why rejection hurts: a common neural alarm system for physical and social pain , 2004, Trends in Cognitive Sciences.

[24]  K. Macdonald,et al.  The peptide that binds: a systematic review of oxytocin and its prosocial effects in humans. , 2010, Harvard review of psychiatry.

[25]  K. Kendrick,et al.  Oxytocin makes females, but not males, less forgiving following betrayal of trust. , 2014, The international journal of neuropsychopharmacology.

[26]  J. Abela,et al.  Key Dimensions and Validity of the Chinese Version of the Individualism-Collectivism Scale , 2013 .

[27]  R. Baumeister,et al.  Does Social Exclusion Motivate Interpersonal Reconnection ? Resolving the “ Porcupine Problem ” , 2006 .

[28]  Keith M. Kendrick,et al.  Prosocial effects of oxytocin and clinical evidence for its therapeutic potential , 2011, Frontiers in Neuroendocrinology.

[29]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[30]  Ulrike Ehlert,et al.  Intranasal Oxytocin Increases Positive Communication and Reduces Cortisol Levels During Couple Conflict , 2009, Biological Psychiatry.

[31]  Reginald B. Adams,et al.  I feel your pain: Emotional closeness modulates neural responses to empathically experienced rejection , 2011, Social neuroscience.

[32]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[33]  K. Williams,et al.  Bulletin Personality and Social Psychology Need Threat Can Motivate Performance after Ostracism on Behalf Of: Society for Personality and Social Psychology , 2022 .

[34]  G. Pagnoni,et al.  Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans , 2014, Brain Imaging and Behavior.

[35]  S. Baron-Cohen,et al.  The Autism-Spectrum Quotient (AQ): Evidence from Asperger Syndrome/High-Functioning Autism, Malesand Females, Scientists and Mathematicians , 2001, Journal of autism and developmental disorders.

[36]  Martin K. Schwarz,et al.  Evoked Axonal Oxytocin Release in the Central Amygdala Attenuates Fear Response , 2012, Neuron.

[37]  W. Maier,et al.  Oxytocin facilitates the sensation of social stress , 2014, Human brain mapping.

[38]  Giuseppe Pagnoni,et al.  Effects of oxytocin and vasopressin on the neural response to unreciprocated cooperation within brain regions involved in stress and anxiety in men and women , 2016, Brain Imaging and Behavior.

[39]  M. Bakermans-Kranenburg,et al.  Does intranasal oxytocin promote prosocial behavior to an excluded fellow player? A randomized-controlled trial with Cyberball , 2013, Psychoneuroendocrinology.

[40]  P. Falkai,et al.  Social Exclusion Leads to Divergent Changes of Oxytocin Levels in Borderline Patients and Healthy Subjects , 2014, Psychotherapy and Psychosomatics.

[41]  K. Williams,et al.  Cyberball: A program for use in research on interpersonal ostracism and acceptance , 2006, Behavior research methods.

[42]  M. Bond,et al.  How Does Cultural Collectivism Operate? , 1982 .

[43]  Peter Kirsch,et al.  Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans , 2005, The Journal of Neuroscience.

[44]  Giuseppe Pagnoni,et al.  Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men , 2012, Psychoneuroendocrinology.

[45]  W. Jung,et al.  Reliability Generalization of Scores on the Spielberger State-Trait Anxiety Inventory , 2002 .

[46]  J. Wagner,et al.  Individualism-Collectivism: Concept and Measure , 1986 .

[47]  B. Averbeck,et al.  CSF and Blood Oxytocin Concentration Changes following Intranasal Delivery in Macaque , 2014, PloS one.

[48]  G. Parker,et al.  Development of a scale to measure interpersonal sensitivity. , 1989, The Australian and New Zealand journal of psychiatry.

[49]  Peter Klaver,et al.  Oxytocin Makes a Face in Memory Familiar , 2009, The Journal of Neuroscience.

[50]  L. Hanson,et al.  Intranasal drug targeting of hypocretin-1 (orexin-A) to the central nervous system. , 2009, Journal of pharmaceutical sciences.

[51]  Angela Sirigu,et al.  Promoting social behavior with oxytocin in high-functioning autism spectrum disorders , 2010, Proceedings of the National Academy of Sciences.

[52]  K. Williams,et al.  Cyberostracism: effects of being ignored over the Internet. , 2000, Journal of personality and social psychology.

[53]  M. Leary,et al.  Why does social exclusion hurt? The relationship between social and physical pain. , 2005, Psychological bulletin.

[54]  Ethan Kross,et al.  Social rejection shares somatosensory representations with physical pain , 2011, Proceedings of the National Academy of Sciences.

[55]  Ulrike Ehlert,et al.  Sex-specific effects of intranasal oxytocin on autonomic nervous system and emotional responses to couple conflict. , 2013, Social cognitive and affective neuroscience.

[56]  S. Hofmann,et al.  Rejection : Applying a Research Domain Criteria Framework to Social Anxiety Attachment Style Moderates the Effects of Oxytocin on Social Behaviors and Cognitions During Social , 2014 .

[57]  N. Toschi,et al.  Brain oxytocin inhibits the (re)activity of the hypothalamo–pituitary–adrenal axis in male rats: involvement of hypothalamic and limbic brain regions , 2000, Regulatory Peptides.

[58]  A. Beck,et al.  Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation , 1988 .

[59]  L. F. Barrett,et al.  Gender differences in oxytocin-associated disruption of decision bias during emotion perception , 2014, Psychiatry Research.

[60]  W. H. Jones,et al.  Psychometric Properties of the Revised Cheek and Buss Shyness Scale , 2005, Journal of personality assessment.

[61]  Kimberly Matheson,et al.  Distress of ostracism: oxytocin receptor gene polymorphism confers sensitivity to social exclusion. , 2015, Social cognitive and affective neuroscience.

[62]  A. Guastella,et al.  Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research , 2013, Psychoneuroendocrinology.

[63]  A. Guastella,et al.  Acute effects of intranasal oxytocin on subjective and behavioral responses to social rejection. , 2010, Experimental and clinical psychopharmacology.

[64]  D. Slattery,et al.  Oxytocin in General Anxiety and Social Fear: A Translational Approach , 2016, Biological Psychiatry.

[65]  R. Baumeister,et al.  The need to belong: desire for interpersonal attachments as a fundamental human motivation. , 1995, Psychological bulletin.

[66]  Frances S. Chen,et al.  Common oxytocin receptor gene (OXTR) polymorphism and social support interact to reduce stress in humans , 2011, Proceedings of the National Academy of Sciences.

[67]  C. Kirschbaum,et al.  Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress , 2003, Biological Psychiatry.

[68]  I. Neumann Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo-pituitary-adrenal axis. , 2002, Progress in brain research.

[69]  Wang Yanfei,et al.  Revision of the Positive Affect and Negative Affect Scale , 2008 .

[70]  Shelley E. Taylor,et al.  Culture, distress, and oxytocin receptor polymorphism (OXTR) interact to influence emotional support seeking , 2010, Proceedings of the National Academy of Sciences.

[71]  D. Frey,et al.  The Different Behavioral Intentions of Collectivists and Individualists in Response to Social Exclusion , 2015, Personality & social psychology bulletin.