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Brain Activity Dissociates Mentalization from Motivation During an Interpersonal Competitive Game

  • Michal Assaf
  • Itamar Kahn
  • Godfrey D. Pearlson
  • Matthew R. Johnson
  • Yehezkel Yeshurun
  • Vince D. Calhoun
  • Talma Hendler
Article

Abstract

Studies demonstrating selective brain networks subserving motivation and mentalization (i.e. attributing states of mind to others) during social interactions have not investigated their mutual independence. We report the results of two fMRI studies using a competitive game requiring players to use implicit ‘on-line’ mentalization simultaneously with motivational processes of gains and losses in playing against a human or a computer opponent. We delineate a network, consisting of bilateral temporoparietal junction, temporal pole (TP), medial prefrontal cortex (MPFC) and right fusiform gyrus, which is sensitive to the opponent’s response (challenging>not challenging the player) and opponent type (human>computer). This network is similar to a known explicit ‘off-line’ mentalization circuit, suggesting its additional involvement in implicit ‘on-line’ mentalization, a process more applicable to real-life social interactions. Importantly, only MPFC and TP were selective to mentalization compared to motivation, highlighting their specific operation in attributing states of mind to others during social interactions.

Keywords

Theory of mind Reward Medial prefrontal cortex Temporoparietal junction Temporal pole 

Notes

Acknowledgements

The authors would like to thank Drs. Kristen McKiernan Miller, Michael Stevens and Brian Knutson for their helpful comments on earlier versions of the manuscript. This work was partially supported by a Hartford Hospital grant (PI: M. Assaf).

References

  1. Adolphs, R. (2003). Cognitive neuroscience of human social behaviour. Nature Reviews. Neuroscience, 4, 165–178. doi: 10.1038/nrn1056.PubMedCrossRefGoogle Scholar
  2. Amodio, D., & Frith, C. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews. Neuroscience, 7, 268–277. doi: 10.1038/nrn1884.PubMedCrossRefGoogle Scholar
  3. Beauchamp, M. S., Lee, K. E., Argall, B. D., & Martin, A. (2004). Integration of auditory and visual information about objects in superior temporal sulcus. Neuron, 41, 809–823. doi: 10.1016/S0896-6273(04)00070-4.PubMedCrossRefGoogle Scholar
  4. Buckner, R. L., & Carroll, D. C. (2007). Self-projection and the brain. Trends in Cognitive Sciences, 11, 49–57. doi: 10.1016/j.tics.2006.11.004.PubMedCrossRefGoogle Scholar
  5. Bunge, S. A. (2004). How we use rules to select actions: a review of evidence from cognitive neuroscience. Cognitive, Affective & Behavioral Neuroscience, 4, 564–579.CrossRefGoogle Scholar
  6. Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., et al. (2002). Dorsal anterior cingulate cortex: a role in reward-based decision making. Proceedings of the National Academy of Sciences of the United States of America, 99, 523–528. doi: 10.1073/pnas.012470999.PubMedCrossRefGoogle Scholar
  7. Castelli, F., Happe, F., Frith, U., & Frith, C. (2000). Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. NeuroImage, 12, 314–325. doi: 10.1006/nimg.2000.0612.PubMedCrossRefGoogle Scholar
  8. Dale, A. M., & Buckner, R. L. (1997). Selective averaging of rapidly presented individual trials using fMRI. Human Brain Mapping, 5, 329–340. doi: 10.1002/(SICI)1097-0193(1997)5:5<329::AID-HBM1>3.0.CO;2-5.CrossRefGoogle Scholar
  9. Delgado, M. R., Frank, R. H., & Phelps, E. A. (2005). Perceptions of moral character modulate the neural systems of reward during the trust game. Nature Neuroscience, 8, 1611–1618. doi: 10.1038/nn1575.PubMedCrossRefGoogle Scholar
  10. Delgado, M. R., Nystrom, L. E., Fissell, C., Noll, D. C., & Fiez, J. A. (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology, 84, 3072–3077.PubMedGoogle Scholar
  11. Dolan, R. J. (2002). Emotion, cognition, and behavior. Science, 298, 1191–1194. doi: 10.1126/science.1076358.PubMedCrossRefGoogle Scholar
  12. First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2002). Structured Clinical Interview for DSM-IV-TR axis I disorders, research version, patient edition. (SCID-I/P). New York: Biometrics Research, New York State Psychiatric Institute.Google Scholar
  13. Friston, K. J., Ashburner, J., Frith, C. D., Poline, J. B., Heather, J. D., & Frackowiak, R. S. J. (1995). Spatial registration and normalization of images. Human Brain Mapping, 3, 165–189. doi: 10.1002/hbm.460030303.CrossRefGoogle Scholar
  14. Frith, U., & Frith, C. D. (2003). Development and neurophysiology of mentalizing. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358, 459–473. doi: 10.1098/rstb.2002.1218.PubMedCrossRefGoogle Scholar
  15. Gallagher, H. L., Jack, A. I., Roepstorff, A., & Frith, C. D. (2002). Imaging the intentional stance in a competitive game. NeuroImage, 16, 814–821. doi: 10.1006/nimg.2002.1117.PubMedCrossRefGoogle Scholar
  16. Genovese, C. R., Lazar, N. A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage, 15, 870–878. doi: 10.1006/nimg.2001.1037.PubMedCrossRefGoogle Scholar
  17. Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4, 223–233. doi: 10.1016/S1364-6613(00)01482-0.PubMedCrossRefGoogle Scholar
  18. Kahn, I., Yeshurun, Y., Rotshtein, P., Fried, I., Ben-Bashat, D., & Hendler, T. (2002). The role of the amygdala in signaling prospective outcome of choice. Neuron, 33, 983–994. doi: 10.1016/S0896-6273(02)00626-8.PubMedCrossRefGoogle Scholar
  19. Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. The Journal of Neuroscience, 17, 4302–4311.PubMedGoogle Scholar
  20. King-Casas, B., Tomlin, D., Anen, C., Camerer, C. F., Quartz, S. R., & Montague, P. R. (2005). Getting to know you: reputation and trust in a two-person economic exchange. Science, 308, 78–83. doi: 10.1126/science.1108062.PubMedCrossRefGoogle Scholar
  21. Knutson, B., Fong, G. W., Bennett, S. M., Adams, C. M., & Hommer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. NeuroImage, 18, 263–272. doi: 10.1016/S1053-8119(02)00057-5.PubMedCrossRefGoogle Scholar
  22. Lane, R. D., Fink, G. R., Chau, P. M. L., & Dolan, R. J. (1997). Neural activation during selective attention to subjective emotional responses. Neuroreport, 8, 3969–3972. doi: 10.1097/00001756-199712220-00024.PubMedCrossRefGoogle Scholar
  23. Lieberman, M. D. (2007). Social cognitive neuroscience: a review of core processes. Annual Review of Psychology, 58, 259–289. doi: 10.1146/annurev.psych.58.110405.085654.PubMedCrossRefGoogle Scholar
  24. McCabe, K., Houser, D., Ryan, L., Smith, V., & Trouard, T. (2001). A functional imaging study of cooperation in two-person reciprocal exchange. Proceedings of the National Academy of Sciences of the United States of America, 98, 11832–11835. doi: 10.1073/pnas.211415698.PubMedCrossRefGoogle Scholar
  25. Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202. doi: 10.1146/annurev.neuro.24.1.167.PubMedCrossRefGoogle Scholar
  26. Ochsner, K. N., & Gross, J. J. (2005). The cognitive control of emotion. Trends in Cognitive Sciences, 9, 242–249. doi: 10.1016/j.tics.2005.03.010.PubMedCrossRefGoogle Scholar
  27. O’Doherty, J. P. (2004). Reward representations and reward-related learning in the human brain: Insights from neuroimaging. Current Opinion in Neurobiology, 14, 769–776. doi: 10.1016/j.conb.2004.10.016.PubMedCrossRefGoogle Scholar
  28. Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16, 331–348. doi: 10.1006/nimg.2002.1087.PubMedCrossRefGoogle Scholar
  29. Pochon, J. B., Levy, R., Fossati, P., Lehericy, S., Poline, J. B., Pillon, B., et al. (2002). The neural system that bridges reward and cognition in humans: an fMRI study. Proceedings of the National Academy of Sciences of the United States of America, 99, 5669–5674. doi: 10.1073/pnas.082111099.PubMedCrossRefGoogle Scholar
  30. Ressler, N. (2004). Rewards and punishments, goal-directed behavior and consciousness. Neuroscience and Biobehavioral Reviews, 28, 27–39. doi: 10.1016/j.neubiorev.2003.10.003.PubMedCrossRefGoogle Scholar
  31. Rilling, J., Gutman, D., Zeh, T., Pagnoni, G., Berns, G., & Kilts, C. (2002). A neural basis for social cooperation. Neuron, 35, 395–405. doi: 10.1016/S0896-6273(02)00755-9.PubMedCrossRefGoogle Scholar
  32. Rilling, J. K., Sanfey, A. G., Aronson, J. A., Nystrom, L. E., & Cohen, J. D. (2004). The neural correlates of theory of mind within interpersonal interactions. NeuroImage, 22, 1694–1703. doi: 10.1016/j.neuroimage.2004.04.015.PubMedCrossRefGoogle Scholar
  33. Rotshtein, P., Henson, R. N., Treves, A., Driver, J., & Dolan, R. J. (2005). Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nature Neuroscience, 8, 107–113. doi: 10.1038/nn1370.PubMedCrossRefGoogle Scholar
  34. Rutkowski, R. G., & Weinberger, N. M. (2005). Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. Proceedings of the National Academy of Sciences of the United States of America, 102, 13664–13669. doi: 10.1073/pnas.0506838102.PubMedCrossRefGoogle Scholar
  35. Sanfey, A. G., Rilling, J. K., Aronson, J. A., Nystrom, L. E., & Cohen, J. D. (2003). The neural basis of economic decision-making in the ultimatum game. Science, 300, 1755–1758. doi: 10.1126/science.1082976.PubMedCrossRefGoogle Scholar
  36. Schultz, R. T. (2005). Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23, 125–141. doi: 10.1016/j.ijdevneu.2004.12.012.PubMedCrossRefGoogle Scholar
  37. Schultz, R. T., Grelotti, D. J., Klin, A., Kleinman, J., Van der Gaag, C., Marois, R., et al. (2003). The role of the fusiform face area in social cognition: implications for the pathobiology of autism. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358, 415–427. doi: 10.1098/rstb.2002.1208.PubMedCrossRefGoogle Scholar
  38. Schmitz, T. W., & Johnson, S. C. (2007). Relevance to self: a brief review and framework of neural systems underlying appraisal. Neuroscience and Biobehavioral Reviews, 31, 585–596. doi: 10.1016/j.neubiorev.2006.12.003.PubMedCrossRefGoogle Scholar
  39. Schultz, W. (2001). Reward signaling by dopamine neurons. The Neuroscientist, 7, 293–302.PubMedGoogle Scholar
  40. Talairach, J., & Tournoux, P. (1988). A co-planar stereotaxic atlas of a human brain. New York: Thieme.Google Scholar
  41. Wright, T. M., Pelphrey, K. A., Allison, T., McKeown, M. J., & McCarthy, G. (2003). Polysensory interactions along lateral temporal regions evoked by audiovisual speech. Cerebral Cortex (New York, N.Y.), 13, 1034–1043. doi: 10.1093/cercor/13.10.1034.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Michal Assaf
    • 1
    • 2
  • Itamar Kahn
    • 3
  • Godfrey D. Pearlson
    • 1
    • 2
  • Matthew R. Johnson
    • 1
    • 4
  • Yehezkel Yeshurun
    • 5
  • Vince D. Calhoun
    • 1
    • 2
    • 7
    • 8
  • Talma Hendler
    • 6
  1. 1.Olin Neuropsychiatry Research CenterInstitute of Living, Hartford HospitalHartfordUSA
  2. 2.Department of PsychiatryYale University School of MedicineNew HavenUSA
  3. 3.Howard Hughes Medical Institute at Harvard UniversityCambridgeUSA
  4. 4.Interdepartmental Neuroscience ProgramYale UniversityNew HavenUSA
  5. 5.School of Computer ScienceTel Aviv UniversityTel AvivIsrael
  6. 6.Functional Brain Research Center, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center and Sackler Faculty of MedicineTel Aviv UniversityTel AvivIsrael
  7. 7.The Mind Research NetworkAlbuquerqueUSA
  8. 8.Department of Electrical and Computer EngineeringThe University of New MexicoAlbuquerqueUSA

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