Temporal characteristics of the influence of punishment on perceptual decision making in the human brain

Journal of Neuroscience

Volumn 33, Issue 9, 2013, Pages 3939-3952

  Blank, Helen ^a,b   Biele, Guido ^d   Heekeren, Hauke R ^a,b,c   Philiastides, Marios G ^e  

^a MAX PLANCK INSTITUTE FOR HUMAN DEVELOPMENT   (Germany)

^b MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d UNIVERSITY OF OSLO   (Norway)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ADULT; ARTICLE; BEHAVIOR; DECISION MAKING; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; EVENT RELATED POTENTIAL; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; PUNISHMENT; RESPONSE TIME; SACCADIC EYE MOVEMENT; TASK PERFORMANCE; VISUAL STIMULATION;

ADULT; BRAIN; BRAIN WAVES; DECISION MAKING; DISCRIMINANT ANALYSIS; DISCRIMINATION (PSYCHOLOGY); ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; PHOTIC STIMULATION; PUNISHMENT; REACTION TIME; SIZE PERCEPTION; SPECTRUM ANALYSIS; YOUNG ADULT;

EID: 84874619458     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4151-12.2013     Document Type: Article

References (112)

1. Anderson BA, Laurent PA, Yantis S (2011) Value-driven attentional capture. Proc Natl Acad Sci U S A 108:10367-10371. CrossRef Medline
2. Andino SL, Michel CM, Thut G, Landis T, de Peralta RG (2005) Prediction of response speed by anticipatory high-frequency (gamma band) oscillations in the human brain. Hum Brain Mapp 24:50-58. CrossRef Medline
3. Basten U, Biele G, Heekeren HR, Fiebach CJ (2010) How the brain integrates costs and benefits during decision making. Proc Natl Acad Sci U S A 107:21767-21772. CrossRef Medline
4. Bennur S, Gold JI (2011) Distinct representations of a perceptual decision and the associated oculomotor plan in the monkey lateral intraparietal area. J Neurosci 31:913-921. CrossRef Medline
5. Blankertz B, Lemm S, Treder M, Haufe S, Müller KR (2011) Single-trial analysis and classification of ERP components-a tutorial. Neuroimage 56:814-825. CrossRef Medline
6. Bogacz R, Brown E, Moehlis J, Holmes P, Cohen JD (2006) The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. Psychol Rev 113:700-765. CrossRef Medline
7. Bogacz R, Hu PT, Holmes PJ, Cohen JD (2010) Do humans produce the speed-accuracy trade-off that maximizes reward rate? Q J Exp Psychol (Hove) 63:863-891. CrossRef Medline
8. Brown H, Friston K, Bestmann S (2011) Active inference, attention, and motor preparation. Front Psychol 2:218. CrossRef Medline
9. Cisek P, Kalaska JF (2010) Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci 33:269-298. CrossRef Medline
10. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulusdriven attention in the brain. Nat Rev Neurosci 3:201-215. Medline
11. Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306-324. CrossRef Medline
12. Dakin SC, Hess RF, Ledgeway T, Achtman RL (2002) What causes nonmonotonic tuning of fMRI response to noisy images? Curr Biol 12:476-477. CrossRef Medline
13. Dambacher M, Hübner R, Schlöosser J (2011) Monetary incentives in speeded perceptual decision: effects of penalizing errors versus slow responses. Front Psychol 2:248. CrossRef Medline
14. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9-21. CrossRef Medline
15. Desimone R, Duncan J (1995) Neural mechanisms of selective visualattention. Annu Rev Neurosci 18:193-222. CrossRef Medline
16. Diederich A (2008) A further test of sequential-sampling models that account for payoff effects on response bias in perceptual decision tasks. Percept Psychophys 70:229-256. CrossRef Medline
17. Diederich A, Busemeyer JR (2006) Modeling the effects of payoff on response bias in a perceptual discrimination task: bound-change, drift-rate-change, or two-stage-processing hypothesis. Percept Psychophys 68:194-207. CrossRef Medline
18. Ding L, Gold JI (2010) Caudate encodes multiple computations for perceptual decisions. J Neurosci 30:15747-15759. CrossRef Medline
19. Ding L, Gold JI (2012) Neural correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field. Cereb Cortex 22:1052-1067. CrossRef Medline
20. Domenech P, Dreher JC (2010) Decision threshold modulation in the human brain. J Neurosci 30:14305-14317. CrossRef Medline
21. Duda R, Hart P, Stork D (2001) Pattern classification. New York: Wiley.
22. Egner T, Hirsch J (2005) Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information. Nat Neurosci 8:1784-1790. CrossRef Medline
23. Engelmann JB, Damaraju E, Padmala S, Pessoa L (2009) Combined effects of attention and motivation on visual task performance: transient and sustained motivational effects. Front Hum Neurosci 3:4. CrossRef Medline
24. Feng S, Holmes P, Rorie A, Newsome WT (2009) Can monkeys choose optimally when faced with noisy stimuli and unequal rewards? PLoS Comput Biol 5:e1000284. CrossRef Medline
25. Fleming SM (2009) Shaping what we see: pinning down the influence of value on perceptual judgements. Front Hum Neurosci 3:9. CrossRef Medline
26. Fleming SM, Whiteley L, Hulme OJ, Sahani M, Dolan RJ (2010) Effects of category-specific costs on neural systems for perceptual decision-making. J Neurophysiol 103:3238-3247. CrossRef Medline
27. Forstmann BU, Anwander A, Schäfer A, Neumann J, Brown S, Wagenmakers, EJ, Bogacz R, Turner R (2010) Cortico-striatal connections predict control over speed and accuracy in perceptual decision making. Proc Natl Acad Sci U S A 107:15916-15920. CrossRef Medline
28. Gold JI, Shadlen MN (2001) Neural computations that underlie decisions about sensory stimuli. Trends Cogn Sci 5:10-16. CrossRef Medline
29. Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535-574. CrossRef Medline
30. Goldstein RZ, Cottone LA, Jia Z, Maloney T, Volkow ND, Squires NK (2006) The effect of graded monetary reward on cognitive event-related potentials and behavior in young healthy adults. Int J Psychophysiol 62:272-279. CrossRef Medline
31. Gould IC, Rushworth MF, Nobre AC (2011) Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations. J Neurophysiol 105:1318-1326. CrossRef Medline
32. Green N, Biele GP, Heekeren HR (2012) Changes in neural connectivity underlie decision threshold modulation for reward maximization. J Neurosci 32:14942-14950. CrossRef Medline
33. Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324:1207-1210. CrossRef Medline
34. Grentt-Jong T, Woldorff MG (2007) Timing and sequence of brain activity in top-down control of visual-spatial attention. PLoS Biol 5:e12. CrossRef Medline
35. Halgren E, Raij T, Marinkovic K, Jousmäki V, Hari R (2000) Cognitive response profile of the human fusiform face area as determined by MEG. Cereb Cortex 10:69-81. CrossRef Medline
36. Hanslmayr S, Gross J, Klimesch W, Shapiro KL (2011) The role of alpha oscillations in temporal attention. Brain Res Rev 67:331-343. Medline
37. Hare TA, Camerer CF, Knoepfle DT, Rangel A (2010) Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J Neurosci 30:583-590. CrossRef Medline
38. Harris A, Adolphs R, Camerer C, Rangel A (2011) Dynamic construction of stimulus values in the ventromedial prefrontal cortex. PLoS One 6:e21074. CrossRef Medline
39. Heekeren HR, Marrett S, Bandettini PA, Ungerleider LG (2004) A general mechanism for perceptual decision-making in the human brain. Nature 431:859-862. CrossRef Medline
40. Heekeren HR, Marrett S, Ungerleider LG (2008) The neural systems that mediate human perceptual decision making. Nat Rev Neurosci 9:467-479. CrossRef Medline
41. Hickey C, van Zoest W, Theeuwes J (2010) The time course of exogenous and endogenous control of covert attention. Exp Brain Res 201:789-796. CrossRef Medline
42. Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3:284-291. CrossRef Medline
43. Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284:1158-1161. CrossRef Medline
44. Iyer A, Lindner A, Kagan I, Andersen RA (2010) Motor preparatory activity in posterior parietal cortex is modulated by subjective absolute value. PLoS Biol 8:e1000444. CrossRef Medline
45. Jeffreys DA (1996) Evoked studies of face and object processing. Vis Cogn 3:1-31. CrossRef
46. Kahneman D, Tversky A (1979) Prospect theory: an analysis of decision under risk. Econometrica 47:263-291. CrossRef
47. Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22:751-761. CrossRef Medline
48. Kim H, Shimojo S, O'Doherty JP (2006) Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain. PLoS Biol 4:e233. CrossRef Medline
49. Kim JN, Shadlen MN (1999) Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat Neurosci 2:176-185. CrossRef Medline
50. Kiss M, Driver J, Eimer M (2009) Reward priority of visual target singletons modulates event-related potential signatures of attentional selection. Psychol Sci 20:245-251. CrossRef Medline
51. Klein-Flügge MC, Bestmann S (2012) Time-dependent changes in human corticospinal excitability reveal value-based competition for action during decision processing. J Neurosci 32:8373-8382. CrossRef Medline
52. Knutson B, Cooper JC (2005) Functional magnetic resonance imaging of reward prediction. Curr Opin Neurol 18:411-417. CrossRef Medline
53. Knutson B, Greer SM (2008) Anticipatory affect: neural correlates and consequences for choice. Philos Trans R Soc B Biol Sci 363:3771-3786. CrossRef Medline
54. Laufer O, Paz R (2012) Monetary loss alters perceptual thresholds and compromises future decisions via amygdala and prefrontal networks. J Neurosci 32:6304-6311. CrossRef Medline
55. Liston DB, Stone LS (2008) Effects of prior information and reward on oculomotor and perceptual choices. J Neurosci 28:13866-13875. CrossRef Medline
56. Litt A, Plassmann H, Shiv B, Rangel A (2011) Dissociating valuation and saliency signals during decision-making. Cereb Cortex 21:95-102. CrossRef Medline
57. Liu J, Higuchi M, Marantz A, Kanwisher N (2000) The selectivity of the occipitotemporal M170 for faces. Neuroreport 11:337-341. CrossRef Medline
58. Liu T, Pleskac TJ (2011) Neural correlates of evidence accumulation in a perceptual decision task. J Neurophysiol 106:2383-2398. CrossRef Medline
59. Louie K, Grattan LE, Glimcher PW (2011) Reward value-based gain control: divisive normalization in parietal cortex. J Neurosci 31:10627-10639. CrossRef Medline
60. Makeig S, Müller MM, Rockstroh B (1996) Effects of voluntary movements on early auditory brain responses. Exp Brain Res 110:487-492. CrossRef Medline
61. Makeig S, Westerfield M, Jung TP, Covington J, Townsend J, Sejnowski TJ, Courchesne E (1999) Functionally independent components of the late positive event-related potential during visual spatial attention. J Neurosci 19:2665-2680. Medline
62. Maunsell JH (2004) Neuronal representations of cognitive state: reward or attention? Trends Cogn Sci 8:261-265. CrossRef Medline
63. Mazza V, Turatto M, Caramazza A (2009) Attention selection, distractor suppression and N2pc. Cortex 45:879-890. CrossRef Medline
64. Mulder MJ, Wagenmakers EJ, Ratcliff R, Boekel W, Forstmann BU (2012) Bias in the brain: a diffusion model analysis of prior probability and potential payoff. J Neurosci 32:2335-2343. CrossRef Medline
65. Murty VP, Labar KS, Adcock RA (2012) Threat of punishment motivates memory encoding via amygdala, not midbrain, interactions with the medial temporal lobe. J Neurosci 32:8969-8976. CrossRef Medline
66. Nomoto K, Schultz W, Watanabe T, Sakagami M (2010) Temporally extended dopamine responses to perceptually demanding rewardpredictive stimuli. J Neurosci 30:10692-10702. CrossRef Medline
67. 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. CrossRef Medline
68. Otto TU, Mamassian P (2012) Noise and correlations in parallel perceptual decision making. Curr Biol 22:1391-1396. CrossRef Medline
69. Parra LC, Spence CD, Gerson AD, Sajda P (2005) Recipes for the linear analysis of EEG. Neuroimage 28:326-341. CrossRef Medline
70. Parra L, Alvino C, Tang A, Pearlmutter B, Yeung N, Osman A, Sajda P (2002) Linear spatial integration for single-trial detection in encephalography. Neuroimage 17:223-230. CrossRef Medline
71. Peck CJ, Jangraw DC, Suzuki M, Efem R, Gottlieb J (2009) Reward modulates attention independently of action value in posterior parietal cortex. J Neurosci 29:11182-11191. CrossRef Medline
72. Pessoa L (2009) How do emotion and motivation direct executive control? Trends Cogn Sci 13:160-166. CrossRef Medline
73. Pessoa L, Engelmann JB (2010) Embedding reward signals into perception and cognition. Front Neurosci 4:17. CrossRef Medline
74. Philiastides MG, Sajda P (2006a) Causal influences in the human brain during face discrimination: a short-window directed transfer function approach. IEEE Trans Biomed Eng 53:2602-2605. CrossRef Medline
75. Philiastides MG, Sajda P (2006b) Temporal characterization of the neural correlates of perceptual decision making in the human brain. Cereb Cortex 16:509-518. CrossRef Medline
76. Philiastides MG, Sajda P (2007) EEG-informed fMRI reveals spatiotemporal characteristics of perceptual decision making. J Neurosci 27:13082-13091. CrossRef Medline
77. Philiastides MG, Ratcliff R, Sajda P (2006) Neural representation of task difficulty and decision making during perceptual categorization: a timing diagram. J Neurosci 26:8965-8975. CrossRef Medline
78. Philiastides MG, Auksztulewicz R, Heekeren HR, Blankenburg F (2011) Causal role of dorsolateral prefrontal cortex in human perceptual decision making. Curr Biol 21:980-983. CrossRef Medline
79. Philiastides MG, Biele G, Heekeren HR (2010) A mechanistic account of value computation in the human brain. Proc Natl Acad Sci U S A 107: 9430-9435. CrossRef Medline
80. Pleger B, Blankenburg F, Ruff CC, Driver J, Dolan RJ (2008) Reward facilitates tactile judgments and modulates hemodynamic responses in human primary somatosensory cortex. J Neurosci 28:8161-8168. CrossRef Medline
81. Pleger B, Ruff CC, Blankenburg F, Klöppel S, Driver J, Dolan RJ (2009) Influence of dopaminergically mediated reward on somatosensory decision-making. PLoS Biol 7:e1000164. CrossRef Medline
82. Ploran EJ, Nelson SM, Velanova K, Donaldson DI, Petersen SE, Wheeler ME (2007) Evidence accumulation and the moment of recognition: dissociating perceptual recognition processes using fMRI. J Neurosci 27:11912-11924. CrossRef Medline
83. Ploran EJ, Tremel JJ, Nelson SM, Wheeler ME (2011) High quality but limited quantity perceptual evidence produces neural accumulation in frontal and parietal cortex. Cereb Cortex 21:2650-2662. CrossRef Medline
84. Potts GF (2011) Impact of reward and punishment motivation on behavior monitoring as indexed by the error-related negativity. Int J Psychophysiol 81:324-331. CrossRef Medline
85. Ratcliff R, Philiastides MG, Sajda P (2009) Quality of evidence for perceptual decision making is indexed by trial-to-trial variability of the EEG. Proc Natl Acad Sci U S A 106:6539-6544. CrossRef Medline
86. Roesch MR, Olson CR (2003) Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex. J Neurophysiol 90:1766-1789. CrossRef Medline
87. Romei V, Gross J, Thut G (2010) On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J Neurosci 30:8692-8697. CrossRef Medline
88. Rorie AE, Gao J, McClelland JL, Newsome WT (2010) Integration of sensory and reward information during perceptual decision-making in lateral intraparietal cortex (LIP) of the macaque monkey. PLoS One 5:e9308. CrossRef Medline
89. Rossion B, Joyce CA, Cottrell GW, Tarr MJ (2003) Early lateralization and orientation tuning for face, word, and object processing in the visual cortex. Neuroimage 20:1609-1624. CrossRef Medline
90. Rousseeuw PJ (1987) Silhouettes: a graphical aid to the interpretation and validation of cluster-analysis. J Comput Appl Math 20:53-65. CrossRef
91. Sänger J, Wascher E (2011) The influence of extrinsic motivation on competition-based selection. Behav Brain Res 224:58-64. CrossRef Medline
92. Serences JT (2008) Value-based modulations in human visual cortex. Neuron 60:1169-1181. CrossRef Medline
93. Serences JT, Saproo S (2010) Population response profiles in early visual cortex are biased in favor of more valuable stimuli. J Neurophysiol 104: 76-87. CrossRef Medline
94. Seymour B, Singer T, Dolan R (2007) The neurobiology of punishment. Nat Rev Neurosci 8:300-311. CrossRef Medline
95. Shadlen MN, Newsome WT (2001) Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J Neurophysiol 86: 1916-1936. Medline
96. Shulman GL, Corbetta M, Buckner RL, Raichle ME, Fiez JA, Miezin FM, Petersen SE (1997) Top-down modulation of early sensory cortex. Cereb Cortex 7:193-206. CrossRef Medline
97. Siegel M, Donner TH, Oostenveld R, Fries P, Engel AK (2007) Highfrequency activity in human visual cortex is modulated by visual motion strength. Cereb Cortex 17:732-741. CrossRef Medline
98. Siegel M, Donner TH, Oostenveld R, Fries P, Engel AK (2008) Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron 60:709-719. CrossRef Medline
99. Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121-134. CrossRef Medline
100. Simen P, Contreras D, Buck C, Hu P, Holmes P, Cohen JD (2009) Reward rate optimization in two-alternative decision making: empirical tests of theoretical predictions. J Exp Psychol Human Percept Perform 35:1865-1897. CrossRef Medline
101. Small DM, Gitelman D, Simmons K, Bloise SM, Parrish T, Mesulam MM (2005) Monetary incentives enhance processing in brain regions mediating top-down control of attention. Cereb Cortex 15:1855-1865. CrossRef Medline
102. Summerfield C, Koechlin E (2010) Economic value biases uncertain perceptual choices in the parietal and prefrontal cortices. Front Hum Neurosci 4:208. CrossRef Medline
103. Talmi D, Dayan P, Kiebel SJ, Frith CD, Dolan RJ (2009) Howhumansintegrate the prospects of pain and reward during choice. J Neurosci 29:14617-14626. CrossRef Medline
104. Taylor SE (1991) Asymmetrical effects of positive and negative events: the mobilization-minimization hypothesis. Psychol Bull 110:67-85. CrossRef Medline
105. Tosoni A, Galati G, Romani GL, Corbetta M (2008) Sensory-motor mechanisms in human parietal cortex underlie arbitrary visual decisions. Nat Neurosci 11:1446-1453. CrossRef Medline
106. van Dijk H, Schoffelen JM, Oostenveld R, Jensen O (2008) Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J Neurosci 28:1816-1823. CrossRef Medline
107. Vickery TJ, Chun MM, Lee D (2011) Ubiquity and specificity of reinforcement signals throughout the human brain. Neuron 72:166-177. CrossRef Medline
108. Weil RS, Furl N, Ruff CC, Symmonds M, Flandin G, Dolan RJ, Driver J, Rees G (2010) Rewarding feedback after correct visual discriminations has both general and specific influences on visual cortex. J Neurophysiol 104: 1746-1757. CrossRef Medline
109. Wrase J, Kahnt T, Schlagenhauf F, Beck A, Cohen MX, Knutson B, Heinz A (2007) Different neural systems adjust motor behavior in response to reward and punishment. Neuroimage 36:1253-1262. CrossRef Medline
110. Wyart V, Tallon-Baudry C (2008) Neural dissociation between visual awareness and spatial attention. J Neurosci 28:2667-2679. CrossRef Medline
111. Yeung N, Sanfey AG (2004) Independent coding of reward magnitude and valence in the human brain. J Neurosci 24:6258-6264. CrossRef Medline
112. Zanto TP, Rubens MT, Thangavel A, Gazzaley A (2011) Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat Neurosci 14:656-661. CrossRef Medline