Temporal dynamics of reward processing revealed by magnetoencephalography

Human Brain Mapping

Volumn 32, Issue 12, 2011, Pages 2228-2240

  Doñamayor, Nuria ^a   Marco Pallarés, Josep ^b,c   Heldmann, Marcus ^d   Schoenfeld, M Ariel ^a   Münte, Thomas F ^d  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b UNIVERSITY OF BARCELONA   (Spain)

^c L'Hospitalet de Llobregat   (Spain)

^d UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Feedback related negativity; Loss; Magnetoencephalography; Reward; Time frequency analysis

Indexed keywords

ACTION POTENTIAL; ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; COLOR; DYNAMICS; EVENT RELATED POTENTIAL; FEEDBACK RELATED NEGATIVITY; FEEDBACK SYSTEM; FEMALE; HUMAN; INSULA; LOW RESOLUTION BRAIN ELECTROMAGNETIC TOMOGRAPHY; MAGNETOENCEPHALOGRAPHY; MALE; MONEY; NORMAL HUMAN; POSTERIOR CINGULATE; PRIORITY JOURNAL; REWARD;

ADULT; BRAIN MAPPING; EVOKED POTENTIALS; FEEDBACK, PSYCHOLOGICAL; FEMALE; GAMBLING; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; REWARD; SIGNAL PROCESSING, COMPUTER-ASSISTED; YOUNG ADULT;

EID: 80054820159     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21184     Document Type: Article

References (93)

1. Abler B, Walter H, Erk S ( 2005): Neural correlates of frustration. Neuroreport 16: 669-672.
2. Amiez C, Joseph JP, Procyk E ( 2005): Anterior cingulate error-related activity is modulated by predicted reward. Eur J Neurosci 21: 3447-3452.
3. Badgaiyan RD, Posner MI ( 1998): Mapping the cingulate cortex in response selection and monitoring. Neuroimage 7: 255-260.
4. Başar E, Schürmann M, Başar-Eroglu C, Karakaş S ( 1997): Alpha oscillations in brain functioning: An integrative theory. Int J Psychophysiol 26: 5-29.
5. Başar E, Başar-Eroglu C, Karakaş S, Schürmann M ( 2001): Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int J Psychophysiol 39: 241-248.
6. Bearer EL, Zhang X, Janvelyan D, Boulat B, Jacobs RE ( 2009): Reward circuitry is perturbed in the absence of the serotonin transporter. NeuroImage 46: 1091-1104.
7. Bellebaum C, Daum I ( 2008): Learning-related changes in reward expectancy are reflected in the feedback-related negativity. Eur J Neurosci 27: 1823-1835.
8. Bengtsson SL, Lau HC, Passingham RE ( 2009): Motivation to do well enhances responses to errors and self-monitoring. Cereb Cortex 19: 797-804.
9. Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, Rosen BR ( 2002): Dorsal anterior cingulate cortex: A role in reward-based decision making. Proc Natl Acad Sci USA 99: 523-528.
10. Bussey TJ, Muir JL, Everitt BJ, Robbins TW ( 1997): Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behav Neurosci 111: 920-936.
11. Càmara E, Rodriguez-Fornells A, Münte TF ( 2008): Functional connectivity of reward processing in the brain. Front Hum Neurosci 2: 19.
12. Carp J, Compton RJ ( 2009): Alpha power is influenced by performance errors. Psychophysiology 46: 336-343.
13. Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD ( 1998): Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280: 747-749.
14. Chua HF, González R, Taylor SF, Welsh RC, Liberzon I ( 2009): Decision-related loss: Regret and disappointment. NeuroImage 47: 2031-2040.
15. Cohen MX, Elger CE, Ranganath C ( 2007): Reward expectation modulates feedback-related negativity and EEG spectra. Neuroimage 35: 968-978.
16. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA ( 2000): Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84: 3072-3077.
17. Falkenstein M, Hohnsbein J, Hoormann J, Blanke L ( 1990): Effects of errors in choice reaction task on the ERP under focused and divided attention. In: Brunia CHM, Gaillard AWK, Kok A, editors. Psychophysiological Brain Research. University Press: Tillburg, The Netherlands. pp 192-195.
18. Fishbein DH, Eldreth DL, Hyde C, Matochik JA, London ED, Contoreggi C, Kurian V, Kimes AS, Breeden A, Grant S ( 2005): Risky decision making and the anterior cingulate cortex in abstinent drug abusers and nonusers. Brain Res Cogn Brain Res 23: 119-136.
19. Fuchs M, Wagner M, Kohler T, Wischmann H-A ( 1999): Linear and nonlinear current density reconstructions. J Clin Neurophysiol 16: 267-295.
20. Fujiwara J, Tobler PN, Taira M, Iijima T, Tsutsui K-I ( 2009): Segregated and integrated coding of reward and punishment in the cingulate cortex. J Neurophysiol 101: 3284-3293.
21. Gehring WJ, Willoughby AR ( 2002): The medial frontal cortex and the rapid processing of monetary gains and losses. Science 295: 2279-2282.
22. Gehring WJ, Willoughby AR. 2004. Are all medial frontal negativities created equal? Towards a richer empirical basis for theories of action monitoring. In: Ullsperger M, Falkenstein M, editors. Errors, Conflicts and the Brain. Current Opinions on Performance Monitoring. Leipzig: Max Planck Institute of Cognitive Neuroscience. pp 14-20.
23. Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E ( 1993): A neural system for error detection and compensation. Psychol Sci 4: 385-390.
24. Goyer JP, Woldorff MG, Huettel SA ( 2008): Rapid electrophysiological brain responses are influenced by both valence and magnitude of monetary rewards. J Cogn Neurosci 20: 2058-2069.
25. 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.
26. Hämäläinen M, Ilmoniemi RJ ( 1984): Interpreting Measured Magnetic Fields of the Brain: Estimates of Current Distributions. Helsinki: Helsinki University of Technology. Report nr TKK-F-A559.
27. Hari R, Salmelin R ( 1997): Human cortical oscillations: A neuromagnetic view through the skull. Trends Neurosci 20: 44-49.
28. Hayden BY, Nair AC, McCoy AN, Platt ML ( 2008): Posterior cingulate cortex mediates outcome-contingent allocation of behavior. Neuron 60: 19-25.
29. Hester R, Fassbender C, Garavan H ( 2004): Individual differences in error processing: A review and reanalysis of three event-related fMRI studies using the GO/NOGO task. Cereb Cortex 14: 986-994.
30. Hewig J, Trippe R, Hecht H, Coles MGH, Holroyd CB, Miltner WH ( 2007): Decision-making in Blackjack: An electrophysiological analysis. Cereb Cortex 17: 865-877.
31. 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.
32. Holroyd CB, Coles MGH, Nieuwenhuis S. ( 2002): Medial prefrontal cortex and error potentials. Science 296: 1610-1611; author reply 1610-1611.
33. Holroyd CB, Krigolson OE ( 2007): Reward prediction error signals associated with a modified time estimation task. Psychophysiology 44: 913-917.
34. Holroyd CB, Nieuwenhuis S, Yeung N, Nystrom L, Mars RB, Coles MGH, Cohen JD ( 2004): Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nat Neurosci 7: 497-498.
35. Holroyd CB, Hajcak G, Larsen JT ( 2006): The good, the bad and the neutral: Electrophysiological responses to feedback stimuli. Brain Res 1105: 93-101.
36. Kennerley SW, Wallis JD ( 2009): Evaluating choices by single neurons in the frontal lobe: Outcome value encoded across multiple decision variables. Eur J Neurosci 29: 2061-2073.
37. Kennerley SW, Walton ME, Behrens TEJ, Buckley MJ, Rushworth MFS ( 2006): Optimal decision making and the anterior cingulate cortex. Nat Neurosci 9: 940-947.
38. Khamassi M, Mulder AB, Tabuchi E, Douchamps V, Wiener SI ( 2008): Anticipatory reward signals in ventral striatal neurons of behaving rats. Eur J Neurosci 28: 1849-1866.
39. 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.
40. Liu X, Powell DK, Wang H, Gold BT, Corbly CR, Joseph JE ( 2007): Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J Neurosci 27: 4587-4597.
41. Maddock RJ ( 1999): The retrosplenial cortex and emotion: New insights from functional neuroimaging of the human brain. Trends Neurosci 22: 310-316.
42. Maddock RJ, Garrett AS, Buonocore MH ( 2003): Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Hum Brain Mapp 18: 30-41.
43. Magno E, Foxe JJ, Molholm S, Robertson IH, Garavan H ( 2006): The anterior cingulate and error avoidance. J Neurosci 26: 4769-4773.
44. Marco-Pallarés J, Müller SV, Münte TF ( 2007): Learning by doing: An fMRI study of feedback-related brain activations. Neuroreport 18: 1423-1426.
45. Marco-Pallarés J, Cucurell D, Cunillera T, García R, Andrés-Pueyo A, Münte TF, Rodriguez-Fornells A ( 2008): Human oscillatory activity associated to reward processing in a gambling task. Neuropsychologia 46: 241-248.
46. Maris E, Oostenveld R ( 2007): Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164: 177-190.
47. McCoy AN, Crowley JC, Haghighian G, Dean HL, Platt ML ( 2003): Saccade reward signals in posterior cingulate cortex. Neuron 40: 1031-1040.
48. Menon V, Adleman NE, White CD, Glover GH, Reiss AL ( 2001): Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp 12: 131-143.
49. 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.
50. Moser JS, Simons RF ( 2009): The neural consequences of flip-flopping: The feedback-related negativity and salience of reward prediction. Psychophysiology 46: 313-320.
51. Müller SV, Möller J, Rodriguez-Fornells A, Münte TF ( 2005): Brain potentials related to self-generated and external information used for performance monitoring. Clin Neurophysiol 116: 63-74.
52. Näätänen R, Ilmoniemi RJ, Alho K ( 1994): Magnetoencephalography in studies of human cognitive brain function. Trends Neurosci 17: 389-395.
53. Nichols TE, Holmes AP ( 2002): Nonparametric permutation tests for functional neuroimaging: A primer with examples. Human Brain Mapp 15: 1-25.
54. Nieuwenhuis S, Holroyd CB, Mol N, Coles MGH ( 2004a) Reinforcement-related brain potentials from medial frontal cortex: Origins and functional significance. Neurosci Biobehav Rev 28: 441-448.
55. Nieuwenhuis S, Yeung N, Holroyd CB, Schurger A, Cohen JD ( 2004b) Sensitivity of electrophysiological activity from medial frontal cortex to utilitarian and performance feedback. Cereb Cortex 14: 741-747.
56. Nieuwenhuis S, Slagter HA, von Geusau NJ, Heslenfeld DJ, Holroyd CB ( 2005): Knowing good from bad: Differential activation of human cortical areas by positive and negative outcomes. Eur J Neurosci 21: 3161-3168.
57. Niki H, Watanabe M ( 1979): Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res 171: 213-224.
58. Nishijo H, Yamamoto Y, Ono T, Uwano T, Yamashita J, Yamashima T ( 1997): Single neuron responses in the monkey anterior cingulate cortex during visual discrimination. Neurosci Lett 227: 79-82.
59. O'Doherty J, Critchley H, Deichmann R, Dolan RJ ( 2003): Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci 23: 7931-799.
60. Papo D, Douiri A, Bouchet F, Caverni J-P, Baudonnière P-M, Bourzeix J-C ( 2007a) Modulation of late alpha band oscillations by feedback in a hypothesis testing paradigm. Int J Psychophysiol 63: 110-116.
61. Papo D, Douiri A, Bouchet F, Caverni J-P, Baudonnière P-M, Bourzeix J-C ( 2007b) Time-frequency intracranial source localization of feedback-related EEG activity in hypothesis testing. Cereb Cortex 17: 1314-1322.
62. Pascual-Marqui RD ( 1999): Review of methods for solving the EEG inverse problem. Int J Bioelectromagn 1: 75-86.
63. Pascual-Marqui RD, Michel CM, Lehmann D ( 1994): Low resolution electromagnetic tomography: A new method for localizing electrical activity in the brain. Int J Psychophysiol 18: 49-65.
64. Paulus MP, Rogalsky C, Simmons A, Feinstein JS, Stein MB ( 2003): Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. Neuroimage 19: 1439-1448.
65. Paus T ( 2001): Primate anterior cingulate cortex: Where motor control, drive and cognition interface. Nat Rev Neurosci 2: 417-424.
66. Polezzi D, Lotto L, Daum I, Sartori G, Rumiati R ( 2008): Predicting outcomes of decisions in the brain. Behav Brain Res 187: 116-122.
67. Polezzi D, Sartori G, Rumiati R, Vidotto G, Daum I ( 2010): Brain correlates of risky decision-making. NeuroImage 49: 1886-1894.
68. Preuschoff K, Quartz SR, Bossaerts P ( 2008): Human insula activation reflects risk prediction errors as well as risk. J Neurosci 28: 2745-2752.
69. Qin J, Lee TMC, Han S ( 2009): Theta and alpha oscillations linked to risk identifications. Brain Res 1269: 125-134.
70. Quilodran R, Rothé M, Procyk E ( 2008): Behavioral shifts and action valuation in the anterior. Cingulate Cortex 57: 314-325.
71. Reynolds SM, Zahm DS ( 2005): Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25: 11757-11767.
72. Rippon G. 2006. Electroencephalography. In: Senior C, Russell T, Gazzaniga MS, editors. Methods in Mind. Cambridge, MA: MIT Press. pp 237-262.
73. Robbins TW, Everitt BJ ( 1996): Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol 6: 228-236.
74. Robinson SE. 1989. Environmental noise cancellation for biomagnetic measurements. In: Williamson SJ, Hoke M, Stroink G, Kotani M, editors. Advances in Biomagnetism. New York, NY: Plenum. pp 721-724.
75. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD ( 2003): The neural basis of economic decision-making in the Ultimatum Game. Science 300: 1755-1758.
76. Schultz W, Tremblay L, Hollerman JR ( 2000): Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10: 272-284.
77. Shima K, Tanji J ( 1998): Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282: 1335-1338.
78. Singh KD. 2006. Magnetoencephalography. In: Senior C, Russell T, Gazzaniga MS, editors. Methods in Mind. Cambridge, MA: MIT Press. pp 291-326.
79. Solomyak O, Marantz A ( 2009): Lexical access in early stages of visual word processing: A single-trial correlational MEG study of heteronym recognition. Brain Lang 108: 191-196.
80. Sutton S, Tueting P, Hammer M, Hakerem G. 1978. Evoked potentials and feedback. In: Otto DA, editor. Multidisciplinary Perspectives in Event-Related Potential Research. Washington, DC: United States Government Printing Office. pp 184-188.
81. Tallon-Baudry C, Bertrand O, Delpuech C, Permier J ( 1997): Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. J Neurosci 17: 722-734.
82. Tom SM, Fox CR, Trepel C, Poldrack RA ( 2007): The neural basis of loss aversion in decision-making under risk. Science 315: 515-518.
83. Uutela K, Hämäläinen M, Somersalo E ( 1999): Visualization of magnetoencephalographic data using minimum current estimates. Neuroimage 10: 173-180.
84. van der Helden J, Boksem MAS, Blom JHG. ( 2009): The importance of failure: Feedback-related negativity predicts motor learning efficiency. Cereb Cortex bhp224.
85. van Dijk H, Schoffelen J-M, Oostenveld R, Jensen O ( 2008): Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J Neurosci 28: 1816-1823.
86. van Drongelen W, Yuchtman M, van Veen BD, van Huffelen AC ( 1996): A spatial filtering technique to detect and localize multiple sources in the brain. Brain Topogr 9: 39-49.
87. Vogt BA, Finch DM, Olson CR ( 1992): Functional heterogeneity in cingulate cortex: The anterior executive and posterior evaluative regions. Cereb Cortex 2: 435-443.
88. Wächter T, Lungu OV, Liu T, Willingham DT, Ashe J ( 2009): Differential effect of reward and punishment on procedural learning. J Neurosci 29: 436-443.
89. Wittfoth M, Küstermann E, Fahle M, Herrmann M ( 2008): The influence of response conflict on error processing: Evidence from event-related fMRI. Brain Res 1194: 118-129.
90. Womelsdorf T, Johnston K, Vinck M, Everling S ( 2010): Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors. Proc Natl Acad Sci 107: 5248-5253.
91. Wu Y, Zhou X ( 2009): The P300 and reward valence, magnitude, and expectancy in outcome evaluation. Brain Res 1286: 114-122.
92. Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C ( 2006): Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain. J Neurosci 26: 9530-9537.
93. Yeung N, Sanfey AG ( 2004): Independent coding of reward magnitude and valence in the human brain. J Neurosci 24: 6258-6264.