The role of ventromedial prefrontal cortex and temporo-parietal junction in third-party punishment behavior

Third parties punish, sacrificing personal interests, offenders who violate either fairness or cooperation norms. This behavior is defined altruistic punishment and the degree of punishment typically increases with the severity of the norm violation. An opposite and apparently paradoxical behavior, namely anti-social punishment, is the tendency to spend own money to punish cooperative or fair behaviors. Previous fMRI studies correlated punishment behavior with increased activation of brain areas belonging to the reward system (e.g. the ventromedial prefrontal cortex, VMPFC), the mentalizing (e.g. the temporoparietal junction, TPJ) and central-executive networks. In the present study, we aimed at investigating the causal role of VMPFC and TPJ in punishment behaviors through the application of anodal transcranial direct current stimulation (tDCS). Sixty healthy participants were randomly assigned to three tDCS conditions: (1) anodal tDCS over VMPFC, (2) anodal tDCS over right TPJ (rTPJ), (3) sham stimulation. At the end of the stimulation, participants played a third-party punishment game, consisting in viewing a series of fair or unfair monetary allocations between unknown proposers and recipients. Participants were asked whether and how much they would punish the proposers using their own monetary endowment. To test membership effects, proposers and recipients could be either Italian or Chinese. Anodal tDCS over VMPFC increased altruistic punishment behavior whereas anodal tDCS over rTPJ increased anti-social punishment choices compared with sham condition, while membership did not influence participant's choices. Our results support the idea that the two types of punishment behaviors rely upon different brain regions, suggesting that reward and mentalizing systems underlie, respectively, altruistic and anti-social punishment behaviors.

[1]  M. Nitsche,et al.  Reducing Prejudice Through Brain Stimulation , 2015, Brain Stimulation.

[2]  C. Papagno,et al.  Transcranial direct current stimulation modulates implicit attitudes towards food in eating disorders. , 2019, The International journal of eating disorders.

[3]  Donald W. Pfaff,et al.  Deconstructing and reconstructing theory of mind , 2015, Trends in Cognitive Sciences.

[4]  Ernst Fehr,et al.  Linking Brain Structure and Activation in Temporoparietal Junction to Explain the Neurobiology of Human Altruism , 2012, Neuron.

[5]  L. Zarri,et al.  Power to the People? An Experimental Analysis of Bottom-Up Accountability of Third-Party Institutions , 2015 .

[6]  Pat Barclay Strategies for cooperation in biological markets, especially for humans , 2013 .

[7]  Mark Levine,et al.  Identity and Emergency Intervention: How Social Group Membership and Inclusiveness of Group Boundaries Shape Helping Behavior , 2005, Personality & social psychology bulletin.

[8]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[9]  David De Cremer,et al.  Social value orientations and the strategic use of fairness in ultimatum bargaining , 2004 .

[10]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[11]  Jason P. Mitchell,et al.  Response of Dorsomedial Prefrontal Cortex Predicts Altruistic Behavior , 2012, The Journal of Neuroscience.

[12]  Á. Pascual-Leone,et al.  Diminishing Reciprocal Fairness by Disrupting the Right Prefrontal Cortex , 2006, Science.

[13]  Ernst Fehr,et al.  Disrupting the prefrontal cortex diminishes the human ability to build a good reputation , 2009, Proceedings of the National Academy of Sciences.

[14]  Pat Barclay,et al.  Why Hate the Good Guy? Antisocial Punishment of High Cooperators Is Greater When People Compete To Be Chosen , 2018, Psychological science.

[15]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[16]  Pat Barclay Biological markets and the effects of partner choice on cooperation and friendship , 2016 .

[17]  Yue-jia Luo,et al.  Diffusion of responsibility attenuates altruistic punishment: A functional magnetic resonance imaging effective connectivity study , 2016, Human brain mapping.

[18]  G. di Pellegrino,et al.  Investment and repayment in a trust game after ventromedial prefrontal damage , 2013, Front. Hum. Neurosci..

[19]  Ori Weisel,et al.  “In-Group Love” and “Out-Group Hate” in Repeated Interaction Between Groups , 2012 .

[20]  Morris B Hoffman The Punisher's Brain: The Evolution of Judge and Jury , 2014 .

[21]  P. V. Lange,et al.  Why prosocials exhibit greater cooperation than proselfs: the roles of social responsibility and reciprocity , 2001 .

[22]  N. Bolognini,et al.  Localizing the effects of anodal tDCS at the level of cortical sources: A Reply to Bailey et al., 2015 , 2016, Cortex.

[23]  Alberto Pisoni,et al.  Cognitive Enhancement Induced by Anodal tDCS Drives Circuit-Specific Cortical Plasticity , 2018, Cerebral cortex.

[24]  Susan Whitfield-Gabrieli,et al.  Brain regions for perceiving and reasoning about other people in school-aged children. , 2009, Child development.

[25]  Miriam C. Klein-Flügge,et al.  Selective alteration of human value decisions with medial frontal tDCS is predicted by changes in attractor dynamics , 2016, Scientific Reports.

[26]  Brian A. Nosek,et al.  Understanding and using the implicit association test: I. An improved scoring algorithm. , 2003, Journal of personality and social psychology.

[27]  Hawaii,et al.  Supporting Online Material Materials and Methods Figs. S1 to S6 Tables S1 and S2 Database S1 Antisocial Punishment across Societies , 2022 .

[28]  Aya Ihara,et al.  Selective Increase of Intention-Based Economic Decisions by Noninvasive Brain Stimulation to the Dorsolateral Prefrontal Cortex , 2015, The Journal of Neuroscience.

[29]  Riitta Hari,et al.  Competing with peers: Mentalizing-related brain activity reflects what is at stake , 2009, NeuroImage.

[30]  F. Sambataro,et al.  Group Membership Modulates the Neural Circuitry Underlying Third Party Punishment , 2016, PloS one.

[31]  Colin Camerer,et al.  “Economic man” in cross-cultural perspective: Behavioral experiments in 15 small-scale societies , 2005, Behavioral and Brain Sciences.

[32]  Á. Pascual-Leone,et al.  Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI , 2012, Brain Stimulation.

[33]  Tokiko Harada,et al.  Neural basis of extraordinary empathy and altruistic motivation , 2010, NeuroImage.

[34]  Uta Sailer,et al.  Better you lose than I do: neural networks involved in winning and losing in a real time strictly competitive game , 2015, Scientific Reports.

[35]  S. Shimojo,et al.  Noninvasive remote activation of the ventral midbrain by transcranial direct current stimulation of prefrontal cortex , 2013, Translational Psychiatry.

[36]  H. Hennig-Schmidt,et al.  Why People Reject Advantageous Offers - Non-monotone Strategies in Ultimatum Bargaining , 2008 .

[37]  U. Fischbacher,et al.  The nature of human altruism , 2003, Nature.

[38]  C. Cecchetto,et al.  Anodal transcranial direct current stimulation over left inferior frontal gyrus enhances sentence comprehension , 2018, Brain and Language.

[39]  L Astolfi,et al.  Multiple-Brain Connectivity During Third Party Punishment: an EEG Hyperscanning Study , 2018, Scientific Reports.

[40]  Katia M. Harlé,et al.  The neural mechanisms of affect infusion in social economic decision-making: A mediating role of the anterior insula , 2012, NeuroImage.

[41]  Lorena R. R. Gianotti,et al.  Diminishing parochialism in intergroup conflict by disrupting the right temporo-parietal junction. , 2014, Social cognitive and affective neuroscience.

[42]  Rick K. Wilson,et al.  Confusion or fairness in the field? Rejections in the ultimatum game under the strategy method , 2006 .

[43]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[44]  Ryan O. Murphy,et al.  Measuring Social Value Orientation , 2011, SSRN Electronic Journal.

[45]  R. Saxe,et al.  What gets the attention of the temporo-parietal junction? An fMRI investigation of attention and theory of mind , 2010, Neuropsychologia.

[46]  Hang Ye,et al.  Modulating the Activity of Ventromedial Prefrontal Cortex by Anodal tDCS Enhances the Trustee’s Repayment through Altruism , 2016, Front. Psychol..

[47]  Geoffrey Bird,et al.  Enhancing Social Ability by Stimulating Right Temporoparietal Junction Tdcs of Right Tpj , 2022 .

[48]  Chang-Hwan Im,et al.  COMETS: A MATLAB toolbox for simulating local electric fields generated by transcranial direct current stimulation (tDCS) , 2013, Biomedical Engineering Letters.

[49]  J. Perner,et al.  Neuroscience and Biobehavioral Reviews Fractionating Theory of Mind: a Meta-analysis of Functional Brain Imaging Studies , 2022 .

[50]  Peter Kirsch,et al.  Beyond revenge: Neural and genetic bases of altruistic punishment , 2011, NeuroImage.

[51]  E. Fehr,et al.  The mentalizing network orchestrates the impact of parochial altruism on social norm enforcement , 2012, Human brain mapping.

[52]  Serge A. R. B. Rombouts,et al.  Dissociable brain networks involved in development of fairness considerations: Understanding intentionality behind unfairness , 2011, NeuroImage.

[53]  C. Papagno,et al.  Transcranial magnetic stimulation of medial prefrontal cortex modulates implicit attitudes towards food , 2015, Appetite.

[54]  Jonathan Bendor,et al.  The Evolution of Norms1 , 2001, American Journal of Sociology.

[55]  Á. Pascual-Leone,et al.  Studying the neurobiology of social interaction with transcranial direct current stimulation--the example of punishing unfairness. , 2008, Cerebral cortex.

[56]  C. Frith,et al.  The Neural Basis of Mentalizing , 2006, Neuron.

[57]  E. Ostrom Collective action and the evolution of social norms , 2000, Journal of Economic Perspectives.

[58]  David H. Zald,et al.  The Neural Correlates of Third-Party Punishment , 2008, Neuron.

[59]  V. Klucharev,et al.  Commentary: The Emerging Neuroscience of Third-Party Punishment , 2017, Front. Hum. Neurosci..

[60]  B. Bara,et al.  Third-party punishment: altruistic and anti-social behaviours in in-group and out-group settings , 2016 .

[61]  U. Fischbacher,et al.  Strong reciprocity, human cooperation, and the enforcement of social norms , 2002, Human nature.

[62]  M. Banaji,et al.  Implicit race attitudes predict trustworthiness judgments and economic trust decisions , 2011, Proceedings of the National Academy of Sciences.

[63]  N. Wenderoth,et al.  A technical guide to tDCS, and related non-invasive brain stimulation tools , 2016, Clinical Neurophysiology.

[64]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[65]  Edward T. Bullmore,et al.  Specialization of right temporo-parietal junction for mentalizing and its relation to social impairments in autism , 2011, NeuroImage.

[66]  A. Greenwald,et al.  Measuring individual differences in implicit cognition: the implicit association test. , 1998, Journal of personality and social psychology.

[67]  S. Strang,et al.  Helping or punishing strangers: neural correlates of altruistic decisions as third-party and of its relation to empathic concern , 2015, Front. Behav. Neurosci..

[68]  J. Grafman,et al.  Effective connectivity of brain regions underlying third-party punishment: Functional MRI and Granger causality evidence , 2017, Social neuroscience.

[69]  David De Cremer,et al.  All is well that ends well, at least for proselfs: Emotional reactions to equality violation as a function of social value orientation , 2005 .

[70]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[71]  B. Weber,et al.  The Effect of Oxytocin on Third-Party Altruistic Decisions in Unfair Situations: An fMRI Study , 2016, Scientific Reports.

[72]  Ernst Fehr,et al.  Parochial altruism in humans , 2006, Nature.

[73]  Keith Jensen,et al.  Punishment and spite, the dark side of cooperation , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[74]  B. Weber,et al.  Other-regarding attention focus modulates third-party altruistic choice: An fMRI study , 2017, Scientific Reports.

[75]  J. Elster Social Norms and Economic Theory , 1989, Handbook of Monetary Policy.

[76]  Nikos Nikiforakis,et al.  Punishment and Counter-punishment in Public Good Games: Can We Still Govern Ourselves? , 2005 .

[77]  Jonathan D. Cohen,et al.  The Neural Basis of Economic Decision-Making in the Ultimatum Game , 2003, Science.

[78]  M. Arsalidou,et al.  Brain responses to social norms: Meta‐analyses of fMRI studies , 2018, Human brain mapping.

[79]  U. Fischbacher,et al.  Social value orientation moderates the effects of intuition versus reflection on responses to unfair ultimatum offers , 2017 .

[80]  H. Möller,et al.  Prefrontal Transcranial Direct Current Stimulation Changes Connectivity of Resting-State Networks during fMRI , 2011, The Journal of Neuroscience.

[81]  R. Saxe Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[82]  Donald Hedeker,et al.  Application of Random-Effects Probit Regression Models , 1994 .

[83]  M. Berlingeri,et al.  What is difficult for you can be easy for me. Effects of increasing individual task demand on prefrontal lateralization: A tDCS study , 2018, Neuropsychologia.

[84]  Michael Tomasello,et al.  No third-party punishment in chimpanzees , 2012, Proceedings of the National Academy of Sciences.

[85]  Robert A. Moffitt,et al.  The Uses of Tobit Analysis , 1980 .

[86]  N. Bolognini,et al.  TDCS increases cortical excitability: Direct evidence from TMS–EEG , 2014, Cortex.

[87]  Ernst Fehr,et al.  Third Party Punishment and Social Norms , 2004 .

[88]  Soo Hong Chew,et al.  Computational substrates of social norm enforcement by unaffected third parties , 2016, NeuroImage.

[89]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[90]  K. Fliessbach,et al.  Social Comparison Affects Reward-Related Brain Activity in the Human Ventral Striatum , 2007, Science.

[91]  Attila Szolnoki,et al.  Evolutionary Establishment of Moral and Double Moral Standards through Spatial Interactions , 2010, PLoS Comput. Biol..

[92]  F. Krueger,et al.  The Emerging Neuroscience of Third-Party Punishment , 2016, Trends in Neurosciences.

[93]  Rosalba Morese,et al.  Neural correlates underlying the comprehension of deceitful and ironic communicative intentions , 2017, Cortex.

[94]  G. Roberts,et al.  Cooperators benefit through reputation-based partner choice in economic games , 2010, Biology Letters.

[95]  T. Mappes,et al.  Costly punishment prevails in intergroup conflict , 2011, Proceedings of the Royal Society B: Biological Sciences.

[96]  E. Fehr,et al.  Cooperation and Punishment in Public Goods Experiments , 1999, SSRN Electronic Journal.

[97]  Ernst Fehr,et al.  Human altruism: economic, neural, and evolutionary perspectives , 2004, Current Opinion in Neurobiology.

[98]  P. V. Lange,et al.  The pursuit of joint outcomes and equality in outcomes: An integrative model of social value orientation. , 1999 .

[99]  Shaul Shalvi,et al.  References and Notes Supporting Online Material Materials and Methods Som Text Figs. S1 to S16 References the Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict among Humans , 2022 .

[100]  M. Grueschow,et al.  The precision of value-based choices depends causally on fronto-parietal phase coupling , 2015, Nature Communications.

[101]  Mark H. Davis Interpersonal Reactivity Index , 2011 .

[102]  C. Miniussi,et al.  Medial prefrontal cortex reacts to unfairness if this damages the self: a tDCS study. , 2015, Social cognitive and affective neuroscience.

[103]  David G. Rand,et al.  Third-party punishment as a costly signal of trustworthiness , 2016, Nature.

[104]  J. Henrich,et al.  Costly Punishment Across Human Societies , 2006, Science.

[105]  David Huffman,et al.  Competition Between Organizational Groups: Its Impact on Altruistic and Anti-Social Motivations , 2011, Manag. Sci..

[106]  D. D. de Quervain,et al.  The Neural Basis of Altruistic Punishment , 2004, Science.

[107]  R. Boyd,et al.  Coordinated Punishment of Defectors Sustains Cooperation and Can Proliferate When Rare , 2010, Science.

[108]  Lena Sarp,et al.  The fade-in – Short stimulation – Fade out approach to sham tDCS – Reliable at 1 mA for naïve and experienced subjects, but not investigators , 2012, Brain Stimulation.

[109]  Colin Camerer,et al.  Economic Games Quantify Diminished Sense of Guilt in Patients with Damage to the Prefrontal Cortex , 2009, The Journal of Neuroscience.

[110]  Alan Kirman,et al.  Selfish or selfless? The role of empathy in economics , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[111]  W. Güth,et al.  An experimental analysis of ultimatum bargaining , 1982 .

[112]  Dana Samson,et al.  Left temporoparietal junction is necessary for representing someone else's belief , 2004, Nature Neuroscience.

[113]  E. Wassermann,et al.  A safety screening questionnaire for transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[114]  P. Hammerstein,et al.  Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating , 1994, Behavioral Ecology and Sociobiology.