Experimental Brain Research

, Volume 236, Issue 1, pp 141–151 | Cite as

Correlation of cue-locked FRN and feedback-locked FRN in the auditory monetary incentive delay task

  • Elena Krugliakova
  • Vasily Klucharev
  • Tommaso Fedele
  • Alexey Gorin
  • Aleksandra Kuznetsova
  • Anna Shestakova
Research Article


Reflecting the discrepancy between received and predicted outcomes, the reward prediction error (RPE) plays an important role in learning in a dynamic environment. A number of studies suggested that the feedback-related negativity (FRN) component of an event-related potential, known to be associated with unexpected outcomes, encodes RPEs. While FRN was clearly shown to be sensitive to the probability of outcomes, the effect of outcome magnitude on FRN remains to be further clarified. In studies on the neural underpinnings of reward anticipation and outcome evaluation, a monetary incentive delay (MID) task proved to be particularly useful. We investigated whether feedback-locked FRN and cue-locked dN200 responses recorded during an auditory MID task were sensitive to the probability and magnitude of outcomes. The cue-locked dN200 is associated with the update of information about the magnitude of prospective outcomes. Overall, we showed that feedback-locked FRN was modulated by both the magnitude and the probability of outcomes during an auditory version of MID task, whereas no such effect was found for cue-locked dN200. Furthermore, the cue-locked dN200, which is associated with the update of information about the magnitude of prospective outcomes, correlated with the standard feedback-locked FRN, which is associated with a negative RPE. These results further expand our knowledge on the interplay between the processing of predictive cues that forecast future outcomes and the subsequent revision of these predictions during outcome delivery.


Feedback-related negativity N200 Monetary incentive delay task Electroencephalography 



The study was supported by Grant 16-18-00065 of the Russian Science Foundation.


  1. Agam Y, Hämäläinen MS, Lee AKC, Dyckman KA, Friedman JS, Isom M et al (2011) Multimodal neuroimaging dissociates hemodynamic and electrophysiological correlates of error processing. Proc Natl Acad Sci USA 108:17556–17561. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baker TE, Holroyd CB (2009) Which way do I go? Neural activation in response to feedback and spatial processing in a virtual T-maze. Cereb Cortex 19:1708–1722. CrossRefPubMedGoogle Scholar
  3. Bandura A (1977) Self-efficacy: toward a unifying theory of behavioral change. Psychol Rev 84:191–215CrossRefPubMedGoogle Scholar
  4. Barto AG, Sutton RS (1982) Simulation of anticipatory responses in classical conditioning by a neuron-like adaptive element. Behav Brain Res 4:221–235. CrossRefPubMedGoogle Scholar
  5. Bellebaum C, Polezzi D, Daum I (2010) It is less than you expected: the feedback-related negativity reflects violations of reward magnitude expectations. Neuropsychologia 48:3343–3350. CrossRefPubMedGoogle Scholar
  6. Boersma P (2001) PRAAT, a system for doing phonetics by computer. Glot Int 5:341–345. Google Scholar
  7. Bollen KA, Jackman RW (1985) Regression diagnostics: an expository treatment of outliers and influential cases. Sociol Methods Res 13:510–542. CrossRefGoogle Scholar
  8. Broyd SJ, Richards HJ, Helps SK, Chronaki G, Bamford S, Sonuga-Barke EJS (2012) An electrophysiological monetary incentive delay (e-MID) task: a way to decompose the different components of neural response to positive and negative monetary reinforcement. J Neurosci Methods 209:40–49. CrossRefPubMedGoogle Scholar
  9. Bush RR, Mosteller F (1951) A model for stimulus generalization and discrimination. Psychol Rev 58:413–423. CrossRefPubMedGoogle Scholar
  10. Camerer C, Ho T-H (1999) Experience-weighted attraction learning in normal form games. Econometrica 67:827–874. CrossRefGoogle Scholar
  11. Cohen MX, Elger CE, Ranganath C (2007) Reward expectation modulates feedback-related negativity and EEG spectra. Neuroimage 35:968–978. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cui J-F, Chen Y-H, Wang Y, Shum DHK, Chan RCK (2013) Neural correlates of uncertain decision making: ERP evidence from the Iowa Gambling Task. Front Hum Neurosci 7:776. PubMedPubMedCentralGoogle Scholar
  13. De Pascalis V, Varriale V, D’Antuono L (2010) Event-related components of the punishment and reward sensitivity. Clin Neurophysiol 121:60–76. CrossRefPubMedGoogle Scholar
  14. Doñamayor N, Schoenfeld MA, Münte TF (2012) Magneto- and electroencephalographic manifestations of reward anticipation and delivery. Neuroimage 62:17–29. CrossRefPubMedGoogle Scholar
  15. Dunning JP, Hajcak G (2007) Error-related negativities elicited by monetary loss and cues that predict loss. NeuroReport 18:1875–1878. CrossRefPubMedGoogle Scholar
  16. Düzel E, Bunzeck N, Guitart-Masip M, Wittmann B, Schott BH, Tobler PN (2009) Functional imaging of the human dopaminergic midbrain. Trends Neurosci 32:321–328. CrossRefPubMedGoogle Scholar
  17. Emeric EE, Brown JW, Leslie M, Pouget P, Stuphorn V, Schall JD (2008) Performance monitoring local field potentials in the medial frontal cortex of primates: anterior cingulate cortex. J Neurophysiol 99:759–772. CrossRefPubMedGoogle Scholar
  18. Erev I, Roth AE (1998) Predicting how people play games: reinforcement learning in experimental games with unique, mixed strategy equilibria. Am Econ Rev 88:848–881. Google Scholar
  19. Gehring WJ, Willoughby AR (2002) The medial frontal cortex and the rapid processing of monetary gains and losses. Science 295:2279–2282. CrossRefPubMedGoogle Scholar
  20. Hajcak G, McDonald N, Simons RF (2003) To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. Psychophysiology. 40(6):895–903. CrossRefPubMedGoogle Scholar
  21. Hajcak G, Moser JS, Holroyd CB, Simons RF (2006) The feedback-related negativity reflects the binary evaluation of good versus bad outcomes. Biol Psychol 71:148–154. CrossRefPubMedGoogle Scholar
  22. Hauser TU, Iannaccone R, Stampfli P, Drechsler R, Brandeis D, Walitza S et al (2014) The feedback-related negativity (FRN) revisited: new insights into the localization, meaning and network organization. Neuroimage 84:159–168. CrossRefPubMedGoogle Scholar
  23. Helfinstein SM, Kirwan ML, Benson BE, Hardin MG, Pine DS, Ernst M et al (2013) Validation of a child-friendly version of the monetary incentive delay task. Soc Cogn Affect Neurosci 8:720–726. CrossRefPubMedGoogle Scholar
  24. Holroyd CB, Coles MGH (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109:679–709. CrossRefPubMedGoogle Scholar
  25. Holroyd CB, Hajcak G, Larsen JT (2006) The good, the bad and the neutral: electrophysiological responses to feedback stimuli. Brain Res 1105:93–101. CrossRefPubMedGoogle Scholar
  26. Holroyd CB, Pakzad-Vaezi KL, Krigolson OE (2008) The feedback correct-related positivity: sensitivity of the event-related brain potential to unexpected positive feedback. Psychophysiology 45:688–697. CrossRefPubMedGoogle Scholar
  27. Holroyd CB, Krigolson OE, Lee S (2011) Reward positivity elicited by predictive cues. NeuroReport 22:249–252. CrossRefPubMedGoogle Scholar
  28. Howell GT, Lacroix GL (2012) Decomposing interactions using GLM in combination with the COMPARE, LMATRIX and MMATRIX subcommands in SPSS. Tutor Quant Methods Psychol 8:1–22CrossRefGoogle Scholar
  29. Knutson B, Westdorp A, Kaiser E, Hommer D (2000) FMRI visualization of brain activity during a monetary incentive delay task. Neuroimage 12:20–27. CrossRefPubMedGoogle Scholar
  30. Knutson B, Fong GW, Bennett SM, Adams CM, Hommer D (2003) A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. Neuroimage 18:263–272. CrossRefPubMedGoogle Scholar
  31. Knutson B, Taylor J, Kaufman M, Peterson R, Glover G (2005) Distributed neural representation of expected value. J Neurosci 25:4806–4812. CrossRefPubMedGoogle Scholar
  32. Kreussel L, Hewig J, Kretschmer N, Hecht H, Coles MGH, Miltner WHR (2012) The influence of the magnitude, probability, and valence of potential wins and losses on the amplitude of the feedback negativity. Psychophysiology 49:207–219. CrossRefPubMedGoogle Scholar
  33. Liao Y, Gramann K, Feng W, Deák GO, Li H (2011) This ought to be good: brain activity accompanying positive and negative expectations and outcomes. Psychophysiology 48:1412–1419. CrossRefPubMedGoogle Scholar
  34. Luu P, Collins P, Tucker DM (2000) Mood, personality, and self-monitoring: negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. J Exp Psychol Gen 129:43–60. CrossRefPubMedGoogle Scholar
  35. Marco-Pallares J, Cucurell D, Cunillera T, García R, Andrés-Pueyo A, Münte TF et al (2008) Human oscillatory activity associated to reward processing in a gambling task. Neuropsychologia 46:241–248. CrossRefPubMedGoogle Scholar
  36. Marco-Pallares J, Cucurell D, Münte TF, Strien N, Rodriguez-Fornells A (2011) On the number of trials needed for a stable feedback-related negativity. Psychophysiology 48:852–860. CrossRefPubMedGoogle Scholar
  37. Miltner WHR, Braun CH, Coles MGH (1997) Event-related brain potentials following incorrect feedback in a time-estimation task: evidence for a “generic” neural system for error detection. J Cogn Neurosci 9:788–798. CrossRefPubMedGoogle Scholar
  38. Nieuwenhuis S, Yeung N, Holroyd CB, Schurger A, Cohen JD (2004) Sensitivity of electrophysiological activity from medial frontal cortex to utilitarian and performance feedback. Cereb Cortex 14:741–747. CrossRefPubMedGoogle Scholar
  39. O’Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews C (2001) Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4:95–102. CrossRefPubMedGoogle Scholar
  40. Oliveira FTP, McDonald JJ, Goodman D (2007) Performance monitoring in the anterior cingulate is not all error related: expectancy deviation and the representation of action-outcome associations. J Cogn Neurosci 19:1994–2004. CrossRefPubMedGoogle Scholar
  41. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442:1042–1045. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Proudfit GH (2015) The reward positivity: from basic research on reward to a biomarker for depression. Psychophysiology 52:449–459. CrossRefPubMedGoogle Scholar
  43. Rademacher L, Salama A, Gründer G, Spreckelmeyer KN (2014) Differential patterns of nucleus accumbens activation during anticipation of monetary and social reward in young and older adults. Soc Cogn Affect Neurosci 9:825–831. CrossRefPubMedGoogle Scholar
  44. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Class Cond II Curr Res Theory 21:64–99. Google Scholar
  45. Sambrook TD, Goslin J (2015) A neural reward prediction error revealed by a meta-analysis of ERPs using great grand averages. Psychol Bull 141:213–235. CrossRefPubMedGoogle Scholar
  46. Schultz W (1997) A neural substrate of prediction and reward. Science (80-.) 275:1593–1599. CrossRefGoogle Scholar
  47. Steele K, Stefansson HO (2015) Decision theory. Stanf Encycl Philos. Google Scholar
  48. Stevens JP (1991) Intermediate statistics: a modern approach. Detecting outliers. PsycCRITIQUES. Google Scholar
  49. Talmi D, Fuentemilla L, Litvak V, Duzel E, Dolan RJ (2012) An MEG signature corresponding to an axiomatic model of reward prediction error. Neuroimage 59:635–645. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Talmi D, Atkinson R, El-Deredy W (2013) The feedback-related negativity signals salience prediction errors, not reward prediction errors. J Neurosci 33:8264–8269. CrossRefPubMedGoogle Scholar
  51. Thomas J, Vanni-Mercier G, Dreher J-C (2013) Neural dynamics of reward probability coding: a magnetoencephalographic study in humans. Front Neurosci 7:214. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Toyomaki A, Murohashi H (2005) Discrepancy between feedback negativity and subjective evaluation in gambling. NeuroReport 16:1865–1868. CrossRefPubMedGoogle Scholar
  53. Ullsperger M, Fischer AG, Nigbur R, Endrass T (2014) Neural mechanisms and temporal dynamics of performance monitoring. Trends Cogn Sci 18:259–267. CrossRefPubMedGoogle Scholar
  54. Von Neumann J, Morgenstern O (1944) Theory of games and economic behavior, vol 625. Princeton University Press, Princeton. Google Scholar
  55. Walsh MM, Anderson JR (2010) Neural correlates of temporal credit assignment. In: 10th International conference on cognitive modeling, ICCM 2010, pp 265–270.
  56. Walsh MM, Anderson JR (2011) Learning from delayed feedback: neural responses in temporal credit assignment. Cogn Affect Behav Neurosci 11:131–143. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Walsh MM, Anderson JR (2012) Learning from experience: event-related potential correlates of reward processing, neural adaptation, and behavioral choice. Neurosci Biobehav Rev 36:1870–1884. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Warren CM, Holroyd CB (2012) The impact of deliberative strategy dissociates ERP components related to conflict processing vs reinforcement learning. Front Neurosci. PubMedPubMedCentralGoogle Scholar
  59. Warren CM, Hyman JM, Seamans JK, Holroyd CB (2015) Feedback-related negativity observed in rodent anterior cingulate cortex. J Physiol Paris 109:87–94. CrossRefPubMedGoogle Scholar
  60. Yeung N, Sanfey AG (2004) Independent coding of reward magnitude and valence in the human brain. J Neurosci 24:6258–6264. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Centre for Cognition and Decision MakingNational Research University Higher School of EconomicsMoscowRussian Federation
  2. 2.Neurosurgery DepartmentUniversity Hospital ZürichZurichSwitzerland

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