Culture and Brain

, Volume 7, Issue 1, pp 67–79 | Cite as

Cultural differences in anterior cingulate cortical response to prediction error

  • Clara S. P. Li
  • Simon Zhornitsky
  • Jaime S. IdeEmail author
Original Research Article


Previous studies have shown cultural differences in the behavioral and neural processes of perspective taking and social emotional processing. It is less clear whether culture influences cognitive functions that do not explicitly involve face perception, group membership or social interactions. Here, we addressed this issue by imaging 29 Asians and 168 European Americans while they performed a stop signal task (SST)—a behavioral paradigm widely used to study cognitive control. In the SST participants responded to a frequent go signal and interrupted their response to an infrequent stop signal. Imaging data were processed by published routines implemented in Statistical Parametric Mapping. Behaviorally Asians and European Americans did not differ in SST performance measures, including the go and stop success rates, go and stop signal reaction time, and the sequential effect, an index of performance monitoring and behavioral adjustment. In a Bayesian model of the SST performance, we identified regional responses to stimulus prediction error (expecting go while encountering stop signal or vice versa) and showed that the dorsal anterior cingulate cortex (dACC) responded to Bayesian prediction error, a surprise signal. Importantly, compared to European Americans, Asians showed higher dACC response to prediction error in a voxelwise analysis examined at a corrected threshold. This finding suggested that, although an increased response to surprise did not impact behavioral performance, Asians appeared to exhibit higher arousal to a salient signal than European Americans, a process likely mediated by midbrain catecholaminergic system. This finding supports racial cultural differences in cognitive and affective processes that go beyond the domains of social emotions, and adds to a growing literature of cultural neuroscience.


Race Cognitive control Bayesian surprise Prediction error FMRI ACC 



This study was supported by NIH grants DA023248 and AA021449. The NIH is otherwise not involved in the design of the experiment, collection and analysis of data, writing, or decision to publish these results.


  1. Alahmadi, N., Evdokimov, S. A., Kropotov, Y. J., Muller, A. M., & Jancke, L. (2016). Different resting state EEG features in children from Switzerland and Saudi Arabia. Frontiers in Human Neuroscience, 10, 559.Google Scholar
  2. Alexander, W. H., & Brown, J. W. (2010). Competition between learned reward and error outcome predictions in anterior cingulate cortex. Neuroimage, 49, 3210–3218.Google Scholar
  3. Andersson, J. L., Hutton, C., Ashburner, J., Turner, R., & Friston, K. (2001). Modeling geometric deformations in EPI time series. Neuroimage, 13, 903–919.Google Scholar
  4. Ashburner, J., & Friston, K. J. (1999). Nonlinear spatial normalization using basis functions. Human Brain Mapping, 7, 254–266.Google Scholar
  5. Ashburner, J., & Friston, K. J. (2005). Unified segmentation. Neuroimage, 26, 839–851.Google Scholar
  6. Behrens, T. E., Woolrich, M. W., Walton, M. E., & Rushworth, M. F. (2007). Learning the value of information in an uncertain world. Nature Neuroscience, 10, 1214–1221.Google Scholar
  7. Berlingeri, M., Gallucci, M., Danelli, L., Forgiarini, M., Sberna, M., & Paulesu, E. (2016). Guess who’s coming to dinner: Brain signatures of racially biased and politically correct behaviors. Neuroscience, 332, 231–241.Google Scholar
  8. Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624–652.Google Scholar
  9. Brown, J. W., & Braver, T. S. (2005). Learned predictions of error likelihood in the anterior cingulate cortex. Science, 307, 1118–1121.Google Scholar
  10. Cao, Y., Contreras-Huerta, L. S., McFadyen, J., & Cunnington, R. (2015). Racial bias in neural response to others’ pain is reduced with other-race contact. Cortex, 70, 68–78.Google Scholar
  11. Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science, 301, 386–389.Google Scholar
  12. Chand, G. B., Wu, J., Qiu, D., & Hajjar, I. (2017). Racial differences in insular connectivity and thickness and related cognitive impairment in hypertension. Frontiers in aging neuroscience, 9, 177.Google Scholar
  13. Chekroud, A. M., Everett, J. A., Bridge, H., & Hewstone, M. (2014). A review of neuroimaging studies of race-related prejudice: does amygdala response reflect threat? Frontiers in Human Neuroscience, 8, 179.Google Scholar
  14. Cheon, B. K., Im, D. M., Harada, T., Kim, J. S., Mathur, V. A., Scimeca, J. M., et al. (2013). Cultural modulation of the neural correlates of emotional pain perception: the role of other-focusedness. Neuropsychologia, 51, 1177–1186.Google Scholar
  15. Cheon, B. K., Livingston, R. W., Hong, Y. Y., & Chiao, J. Y. (2014). Gene x environment interaction on intergroup bias: The role of 5-HTTLPR and perceived outgroup threat. Social Cognitive and Affective Neuroscience, 9, 1268–1275.Google Scholar
  16. Chiao, J. Y. (2015). Current emotion research in cultural neuroscience. Emotion Review, 7, 280–293.Google Scholar
  17. Chiao, J. Y., Li, S. C., Turner, R., Lee-Tauler, S. Y., & Pringle, B. A. (2017). Cultural neuroscience and global mental health: addressing grand challenges. Culture and Brain, 5, 4–13.Google Scholar
  18. Cloutier, J., Li, T., & Correll, J. (2014). The impact of childhood experience on amygdala response to perceptually familiar black and white faces. Journal of Cognitive Neuroscience, 26, 1992–2004.Google Scholar
  19. Contreras-Huerta, L. S., Baker, K. S., Reynolds, K. J., Batalha, L., & Cunnington, R. (2013). Racial bias in neural empathic responses to pain. PLoS ONE, 8, e84001.Google Scholar
  20. Critchley, H. D. (2002). Electrodermal responses: What happens in the brain. The Neuroscientist : A Review Journal Bringing Neurobiology, Neurology and psyChiatry, 8, 132–142.Google Scholar
  21. Della-Maggiore, V., Chan, W., Peres-Neto, P. R., & McIntosh, A. R. (2002). An empirical comparison of SPM preprocessing parameters to the analysis of fMRI data. Neuroimage, 17, 19–28.Google Scholar
  22. Dunsmoor, J. E., Kubota, J. T., Li, J., Coelho, C. A., & Phelps, E. A. (2016). Racial stereotypes impair flexibility of emotional learning. Social Cognitive and Affective Neuroscience, 11, 1363–1373.Google Scholar
  23. Farr, O. M., Hu, S., Zhang, S., & Li, C. S. (2012). Decreased saliency processing as a neural measure of Barratt impulsivity in healthy adults. Neuroimage, 63, 1070–1077.Google Scholar
  24. Forbes, C. E., Cox, C. L., Schmader, T., & Ryan, L. (2012). Negative stereotype activation alters interaction between neural correlates of arousal, inhibition and cognitive control. Social Cognitive and Affective Neuroscience, 7, 771–781.Google Scholar
  25. Freeman, J. B., Rule, N. O., Adams, R. B., Jr., & Ambady, N. (2009). Culture shapes a mesolimbic response to signals of dominance and subordination that associates with behavior. Neuroimage, 47, 353–359.Google Scholar
  26. Friston, K., Holmes, A. P., Worsley, K. J., Poline, J. B., Frith, C. D., & Frackowiak, R. (1995). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2, 189–210.Google Scholar
  27. Friston, K. J., Josephs, O., Zarahn, E., Holmes, A. P., Rouquette, S., & Poline, J. B. (2000). To smooth or not to smooth? Bias and efficiency in fMRI time-series analysis. Neuroimage, 12, 196–208.Google Scholar
  28. Han, S., & Ma, Y. (2014). Cultural differences in human brain activity: a quantitative meta-analysis. Neuroimage., 1(99), 293–300.Google Scholar
  29. Han, S., Mao, L., Qin, J., Friederici, A. D., & Ge, J. (2011). Functional roles and cultural modulations of the medial prefrontal and parietal activity associated with causal attribution. Neuropsychologia, 49, 83–91.Google Scholar
  30. Hayden, B. Y., Heilbronner, S. R., Pearson, J. M., & Platt, M. L. (2011). Surprise signals in anterior cingulate cortex: neuronal encoding of unsigned reward prediction errors driving adjustment in behavior. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 31, 4178–4187.Google Scholar
  31. Hechtman, L. A., Raila, H., Chiao, J. Y., & Gruber, J. (2013). Positive emotion regulation and psychopathology: A transdiagnostic cultural neuroscience approach. Journal of Experimntal Psychopathology, 4, 502–528.Google Scholar
  32. Holroyd, C. B., Nieuwenhuis, S., Yeung, N., Nystrom, L., Mars, R. B., Coles, M. G., et al. (2004). Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nature Neuroscience, 7, 497–498.Google Scholar
  33. Hu, J., Hu, S., Maisano, J. R., Chao, H. H., Zhang, S., & Li, C. R. (2016). Novelty seeking, harm avoidance, and cerebral responses to conflict anticipation: An exploratory study. Frontiers in Human Neuroscience, 10, 546.Google Scholar
  34. Hu, S., Ide, J. S., Zhang, S., & Li, C. S. (2015). Anticipating conflict: Neural correlates of a Bayesian belief and its motor consequence. Neuroimage, 119, 286–295.Google Scholar
  35. Hu, S., Tseng, Y. C., Winkler, A. D., & Li, C. S. (2014). Neural bases of individual variation in decision time. Human Brain Mapping, 35, 2531–2542.Google Scholar
  36. Hutton, C., Bork, A., Josephs, O., Deichmann, R., Ashburner, J., & Turner, R. (2002). Image distortion correction in fMRI: A quantitative evaluation. Neuroimage, 16, 217–240.Google Scholar
  37. Ide, J. S., Hu, S., Zhang, S., Mujica-Parodi, L. R., & Li, C. S. (2016). Power spectrum scale invariance as a neural marker of cocaine misuse and altered cognitive control. NeuroImage Clinical, 11, 349–356.Google Scholar
  38. Ide, J. S., & Li, C. S. (2011). A cerebellar thalamic cortical circuit for error-related cognitive control. NeuroImage, 54, 455–464.Google Scholar
  39. Ide, J. S., Shenoy, P., Yu, A. J., & Li, C. S. (2013). Bayesian prediction and evaluation in the anterior cingulate cortex. Journal of Neuroscience, 33, 2039–2047.Google Scholar
  40. Jessup, R. K., Busemeyer, J. R., & Brown, J. W. (2010). Error effects in anterior cingulate cortex reverse when error likelihood is high. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30, 3467–3472.Google Scholar
  41. Kim, B., Sung, Y. S., & McClure, S. M. (2012). The neural basis of cultural differences in delay discounting. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 367, 650–656.Google Scholar
  42. Levitt, H. (1971). Transformed up-down methods in psychoacoustics. The Journal of the Acoustical society of America, 49(2B), 467-477.Google Scholar
  43. Li, T., Cardenas-Iniguez, C., Correll, J., & Cloutier, J. (2016). The impact of motivation on race-based impression formation. Neuroimage, 124, 1–7.Google Scholar
  44. Li CS, Chao HH, Lee TW (2009) Neural correlates of speeded as compared with delayed responses in a stop signal task: An indirect analog of risk taking and association with an anxiety trait. In: Cereb Cortex, pp 839-848.Google Scholar
  45. Li, C. S., Huang, C., Constable, R. T., & Sinha, R. (2006). Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. The Journal of neuroscience : the official journal of the Society for Neuroscience, 26, 186–192.Google Scholar
  46. Li, X., Liu, Y., Luo, S., Wu, B., Wu, X., & Han, S. (2015). Mortality salience enhances racial in-group bias in empathic neural responses to others’ suffering. Neuroimage, 118, 376–385.Google Scholar
  47. Liu, G., Allen, B., Lopez, O., Aizenstein, H., Boudreau, R., Newman, A., et al. (2015a). Racial Differences in Gray Matter Integrity by Diffusion Tensor in Black and White Octogenarians. Current Alzheimer Research, 12, 648–654.Google Scholar
  48. Liu, Y., Lin, W., Xu, P., Zhang, D., & Luo, Y. (2015b). Neural basis of disgust perception in racial prejudice. Human Brain Mapping, 36, 5275–5286.Google Scholar
  49. Logan, G. D., Cowan, W. B., & Davis, K. A. (1984a). On the Ability to Inhibit Simple and Choice Reaction-Time Responses - a Model and a Method. J Exp Psychol Human, 10, 276–291.Google Scholar
  50. Logan, G. D., Cowan, W. B., & Davis, K. A. (1984b). On the ability to inhibit simple and choice reaction time responses: a model and a method. Journal of Experimental Psychology: Human Perception and Performance, 10, 276–291.Google Scholar
  51. Long, H., Liu, B., Hou, B., Wang, C., Li, J., Qin, W., et al. (2013). The long rather than the short allele of 5-HTTLPR predisposes Han Chinese to anxiety and reduced connectivity between prefrontal cortex and amygdala. Neurosci Bull, 29, 4–15.Google Scholar
  52. Losin, E. A., Cross, K. A., Iacoboni, M., & Dapretto, M. (2014). Neural processing of race during imitation: self-similarity versus social status. Human Brain Mapping, 35, 1723–1739.Google Scholar
  53. Lu, Q., Zeltzer, L., & Tsao, J. (2013). Multiethnic Differences in Responses to Laboratory Pain Stimuli Among Children. Health Psychology, 32, 905–914.Google Scholar
  54. Manza, P., Hu, S., Chao, H. H., Zhang, S., Leung, H. C., & Li, C. R. (2016). A dual but asymmetric role of the dorsal anterior cingulate cortex in response inhibition and switching from a non-salient to salient action. Neuroimage, 134, 466–474.Google Scholar
  55. Martin, L. E., Potts, G. F., Burton, P. C., & Montague, P. R. (2009). Electrophysiological and hemodynamic responses to reward prediction violation. NeuroReport, 20, 1140–1143.Google Scholar
  56. Molapour, T., Golkar, A., Navarrete, C. D., Haaker, J., & Olsson, A. (2015). Neural correlates of biased social fear learning and interaction in an intergroup context. Neuroimage, 121, 171–183.Google Scholar
  57. Molenberghs, P., Bosworth, R., Nott, Z., Louis, W. R., Smith, J. R., Amiot, C. E., et al. (2014). The influence of group membership and individual differences in psychopathy and perspective taking on neural responses when punishing and rewarding others. Human Brain Mapping, 35, 4989–4999.Google Scholar
  58. Norasakkunkit, V., & Kalick, S. M. (2002). Culture, ethnicity, and emotional distress measures - The role of self-construal and self-enhancement. Journal of Cross-Cultural Psychology, 33, 56–70.Google Scholar
  59. Okazaki, S., Liu, J. F., Longworth, S. L., & Minn, J. Y. (2002). Asian American-white American differences in expressions of social anxiety: a replication and extension. Cultur Divers Ethnic Minor Psychol, 8, 234–247.Google Scholar
  60. Ortega, F., & Vidal, F. (2016). Culture: by the brain and in the brain? Hist Cienc Saude Manguinhos, 23, 965–983.Google Scholar
  61. Osher, Y., Hamer, D., & Benjamin, J. (2000). Association and linkage of anxiety-related traits with a functional polymorphism of the serotonin transporter gene regulatory region in Israeli sibling pairs. Molecular psychiatry, 5, 216–219.Google Scholar
  62. Pornpattananangkul, N., Hariri, A. R., Harada, T., Mano, Y., Komeda, H., Parrish, T. B., et al. (2016). Cultural influences on neural basis of inhibitory control. Neuroimage, 139, 114–126.Google Scholar
  63. Rowell, L. N., Mechlin, B., Ji, E., Addamo, M., & Girdler, S. S. (2011). Asians differ from non-Hispanic Whites in experimental pain sensitivity. European Journal of Pain, 15, 764–771.Google Scholar
  64. Rushworth, M. F., Walton, M. E., Kennerley, S. W., & Bannerman, D. M. (2004). Action sets and decisions in the medial frontal cortex. Trends Cogn Sci, 8, 410–417.Google Scholar
  65. Senholzi, K. B., Depue, B. E., Correll, J., Banich, M. T., & Ito, T. A. (2015). Brain activation underlying threat detection to targets of different races. Social Neuroscience, 10, 651–662.Google Scholar
  66. Seo, H., & Lee, D. (2007). Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game. The Journal of neuroscience : the official journal of the Society for Neuroscience, 27, 8366–8377.Google Scholar
  67. Sessa, P., Meconi, F., Castelli, L., & Dell’Acqua, R. (2014). Taking one’s time in feeling other-race pain: an event-related potential investigation on the time-course of cross-racial empathy. Social cognitive and affective neuroscience, 9, 454–463.Google Scholar
  68. Sheng, F., Liu, Q., Li, H., Fang, F., & Han, S. (2014). Task modulations of racial bias in neural responses to others’ suffering. Neuroimage, 88, 263–270.Google Scholar
  69. Sheng, F., Liu, Y., Zhou, B., Zhou, W., & Han, S. (2013). Oxytocin modulates the racial bias in neural responses to others’ suffering. Biological Psychology, 92, 380–386.Google Scholar
  70. Sue, D., Sue, D. M., & Ino, S. (1990). Assertiveness and social anxiety in Chinese-American women. Journal of Psychology, 124, 155–163.Google Scholar
  71. Sui, J., Hong, Y. Y., Hong Liu, C., Humphreys, G. W., & Han, S. (2013). Dynamic cultural modulation of neural responses to one’s own and friend’s faces. Soc Cogn Affect Neurosci., 8, 326–332.Google Scholar
  72. Telzer, E. H., Flannery, J., Shapiro, M., Humphreys, K. L., Goff, B., Gabard-Durman, L., et al. (2013). Early experience shapes amygdala sensitivity to race: an international adoption design. Journal of Neuroscience, 33, 13484–13488.Google Scholar
  73. Telzer, E. H., Qu, Y., & Lin, L. C. (2017). Neural processes underlying cultural differences in cognitive persistence. Neuroimage, 156, 224–231.Google Scholar
  74. Tsai, J. L. (2017). Ideal affect in daily life: implications for affective experience, health, and social behavior. Curr Opin Psychol, 17, 118–128.Google Scholar
  75. Wang, G., Mao, L., Ma, Y., Yang, X., Cao, J., Liu, X., et al. (2012). Neural representations of close others in collectivistic brains. Soc Cogn Affect Neurosci., 7, 222–229.Google Scholar
  76. Wang, C., Wu, B., Liu, Y., Wu, X., & Han, S. (2015). Challenging emotional prejudice by changing self-concept: priming independent self-construal reduces racial in-group bias in neural responses to other’s pain. Social cognitive and affective neuroscience, 10, 1195–1201.Google Scholar
  77. Wetheril, G. B., Chen, H., & Vasudeva, R. B. (1966). Sequential Estimation of Quantal Response Curves–a New Method of Estimation. Biometrika, 53, 439–454.Google Scholar
  78. Winkler, A. D., Hu, S., & Li, C. S. (2013). The influence of risky and conservative mental sets on cerebral activations of cognitive control. International journal of psychophysiology: official journal of the International Organization of Psychophysiology, 87, 254–261.Google Scholar
  79. Xu, K., & Wang, F. (2013). Influence of 5-HTTLPR genotypes on structural and functional connectivity within amygdala-prefrontal cortex circuitry. Neurosci Bull, 29, 1–2.Google Scholar
  80. Yu, A. J., Dayan, P., & Cohen, J. D. (2009). Dynamics of attentional selection under conflict: toward a rational bayesian account. Journal of Experimental Psychology Human, 35, 700–717.Google Scholar
  81. Zahodne, L. B., Schupf, N., & Brickman, A. M. (2017). Control beliefs are associated with preserved memory function in the face of low hippocampal volume among diverse older adults. Brain Imaging Behavior. Scholar
  82. Zhang, S., Hu, S., Chao, H. H., Ide, J. S., Luo, X., Farr, O. M., et al. (2014). Ventromedial prefrontal cortex and the regulation of physiological arousal. Social Cognitive and Affective Neuroscience, 9, 900–908.Google Scholar
  83. Zhang, S., Hu, S., Chao, H. H., Luo, X., Farr, O. M., & Li, C. S. (2012). Cerebral correlates of skin conductance responses in a cognitive task. Neuroimage, 62, 1489–1498.Google Scholar
  84. Zhang, Y., Ide, J. S., Zhang, S., Hu, S., Valchev, N. S., Tang, X., et al. (2017). Distinct neural processes support post-success and post-error slowing in the stop signal task. Neuroscience, 357, 273–284.Google Scholar
  85. Zhang, S., & Li, C. S. (2010). A neural measure of behavioral engagement: task-residual low-frequency blood oxygenation level-dependent activity in the precuneus. Neuroimage, 49, 1911–1918.Google Scholar
  86. Zhu, Y., Zhang, L., Fan, J., & Han, S. (2007). Neural basis of cultural influence on self-representation. Neuroimage, 34, 1310–1316.Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Phillips AcademyAndoverUSA
  2. 2.Department of PsychiatryYale University School of MedicineNew HavenUSA
  3. 3.Connecticut Mental Health CenterNew HavenUSA

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