Segregated encoding of reward-identity and stimulus-reward associations in human orbitofrontal cortex

Journal of Neuroscience

Volumn 33, Issue 7, 2013, Pages 3202-3211

  Klein Flügge, Miriam Cornelia ^a   Barron, Helen Catharine ^a   Brodersen, Kay Henning ^b   Dolan, Raymond J ^a   John Behrens, Timothy Edward ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ADULT; ARTICLE; BEHAVIOR; BOLD SIGNAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LEARNING; MALE; NORMAL HUMAN; ORBITAL CORTEX; PREDICTION; PRIORITY JOURNAL; RESPONSE TIME; REWARD; VISUAL CORTEX; VISUAL STIMULATION;

ADAPTATION, PSYCHOLOGICAL; ADULT; CUES; DATA INTERPRETATION, STATISTICAL; DECISION MAKING; ECHO-PLANAR IMAGING; FEMALE; FOOD; FRONTAL LOBE; HUMANS; LEARNING; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; ORBIT; OXYGEN; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; REACTION TIME; REWARD; VISUAL CORTEX; YOUNG ADULT;

EID: 84873664606     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2532-12.2013     Document Type: Article

References (53)

1. Balleine BW, Dickinson A (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37:407-419. CrossRef Medline
2. Bar M, Tootell RB, Schacter DL, Greve DN, Fischl B, Mendola JD, Rosen BR, Dale AM (2001) Cortical mechanisms specific to explicit visual object recognition. Neuron 29:529-535. CrossRef Medline
3. Bar M, Kassam KS, Ghuman AS, Boshyan J, Schmid AM, Schmidt AM, Dale AM, Hämäläinen MS, Marinkovic K, Schacter DL, Rosen BR, Halgren E (2006) Top-down facilitation of visual recognition. Proc Natl Acad Sci USA 103:449-454. CrossRef Medline
4. Behrens TE, Woolrich MW, Walton ME, Rushworth MF (2007) Learning the value of information in an uncertain world. Nat Neurosci 10:1214-1221. CrossRef Medline
5. Birn RM, Diamond JB, Smith MA, Bandettini PA (2006) Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31:1536-1548. CrossRef Medline
6. Boorman ED, Behrens TE, Woolrich MW, Rushworth MF (2009) How green is the grass on the other side? Frontopolar cortex and the evidence in favor of alternative courses of action. Neuron 62:733-743. CrossRef Medline
7. Bouret S, Richmond BJ (2010) Ventromedial and orbital prefrontal neurons differentially encode internally and externally driven motivational values in monkeys. J Neurosci 30:8591-8601. CrossRef Medline
8. Burke KA, Franz TM, Miller DN, Schoenbaum G (2008) The role of the orbitofrontal cortex in the pursuit of happiness and more specific rewards. Nature 454:340-344. CrossRef Medline
9. Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371: 179-207. CrossRef Medline
10. Croxson PL, Johansen-Berg H, Behrens TE, Robson MD, Pinsk MA, Gross CG, Richter W, Richter MC, Kastner S, Rushworth MF (2005) Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. J Neurosci 25: 8854-8866. CrossRef Medline
11. Del Parigi A, Gautier J-F, Chen K, Salbe AD, Ravussin E, Reiman E, Tataranni PA (2002) Neuroimaging and obesity: mapping the brain responses to hunger and satiation in humans using positron emission tomography. Ann N Y Acad Sci 967:389-397. Medline
12. Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101: 3270-3283. CrossRef Medline
13. Gallagher M, McMahan RW, Schoenbaum G (1999) Orbitofrontal cortex and representation of incentive value in associative learning. J Neurosci 19:6610-6614. Medline
14. Glover GH, Li TQ, Ress D (2000) Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 44:162-167. CrossRef Medline
15. Gottfried JA, O'Doherty J, Dolan RJ (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301:1104-1107. CrossRef Medline
16. Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci (Regul Ed) 10:14-23. CrossRef Medline
17. Hampton AN, O'Doherty JP (2007) Decoding the neural substrates of reward-related decision making with functional MRI. Proc Natl Acad Sci USA 104:1377-1382. CrossRef Medline
18. Henson RN, Rugg MD (2003) Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia 41: 263-270. CrossRef Medline
19. Hikosaka K, Watanabe M (2000) Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. Cereb Cortex 10:263-271. CrossRef Medline
20. Hunt LT, Kolling N, Soltani A, Woolrich MW, Rushworth MF, Behrens TE (2012) Mechanisms underlying cortical activity during value-guided choice. Nat Neurosci 15:470-476. CrossRef Medline
21. Hutton C, Josephs O, Stadler J, Featherstone E, Reid A, Speck O, Bernarding J, Weiskopf N (2011) The impact of physiological noise correction on fMRI at 7T. Neuroimage 57:101-112. CrossRef Medline
22. Jones BM, White KG (1994) An investigation of the differential-outcomes effect within sessions. J Exp Anal Behav 61:389-406. CrossRef Medline
23. Kahnt T, Chang LJ, Park SQ, Heinzle J, Haynes JD (2012) Connectivitybased parcellation of the human orbitofrontal cortex. J Neurosci 32: 6240-6250. CrossRef Medline
24. McDannald MA, Takahashi YK, Lopatina N, Pietras BW, Jones JL, Schoenbaum G (2012) Model-based learning and the contribution of the orbitofrontal cortex to the model-free world. Eur J Neurosci 35:991-996. CrossRef Medline
25. Noonan MP, Walton ME, Behrens TE, Sallet J, Buckley MJ, Rushworth MF (2010) Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex. Proc Natl Acad Sci U S A 107: 20547-20552. CrossRef Medline
26. Noonan MP, Mars RB, Rushworth MF (2011) Distinct roles of three frontal cortical areas in reward-guided behavior. J Neurosci 31:14399-14412. CrossRef Medline
27. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ (2002) Neural responses during anticipation of a primary taste reward. Neuron 33:815-826. CrossRef Medline
28. Ostlund SB, Balleine BW (2007) Orbitofrontal cortex mediates outcome encoding in Pavlovian but not instrumental conditioning. J Neurosci 27:4819-4825. CrossRef Medline
29. Padoa-Schioppa C (2011) Neurobiology of economic choice: a good-based model. Annu Rev Neurosci 34:333-359. CrossRef Medline
30. Padoa-Schioppa C, Assad JA (2006) Neurons in the orbitofrontal cortex encode economic value. Nature 441:223-226. CrossRef Medline
31. Padoa-Schioppa C, Assad JA (2008) The representation of economic value in the orbitofrontal cortex is invariant for changes of menu. Nat Neurosci 11:95-102. CrossRef Medline
32. Plassmann H, O'Doherty J, Rangel A (2007) Orbitofrontal cortex encodes willingness to pay in everyday economic transactions. J Neurosci 27: 9984-9988. CrossRef Medline
33. Plassmann H, O'Doherty JP, Rangel A (2010) Appetitive and aversive goal values are encoded in the medial orbitofrontal cortex at the time of decision making. J Neurosci 30:10799-10808. CrossRef Medline
34. Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54-71. CrossRef Medline
35. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676-682. CrossRef Medline
36. Rolls ET (2000) The orbitofrontal cortex and reward. Cereb Cortex 10:284-294. CrossRef Medline
37. Rolls ET, Baylis LL (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437-5452. Medline
38. Rolls ET, Critchley HD, Browning AS, Hernadi I, Lenard L (1999) Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J Neurosci 19:1532-1540. Medline
39. Rudebeck PH, Murray EA (2011) Dissociable effects of subtotal lesions within the macaque orbital prefrontal cortex on reward-guided behavior. J Neurosci 31:10569-10578. CrossRef Medline
40. Rudebeck PH, Walton ME, Smyth AN, Bannerman DM, Rushworth MF (2006) Separate neural pathways process different decision costs. Nat Neurosci 9:1161-1168. CrossRef Medline
41. Rushworth MF, Hadland KA, Paus T, Sipila PK (2002) Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. J Neurophysiol 87:2577-2592. Medline
42. Rushworth MF, Noonan MP, Boorman ED, Walton ME, Behrens TE (2011) Frontal cortex and reward-guided learning and decision-making. Neuron 70:1054-1069. CrossRef Medline
43. Savage LM (2001) In search of the neurobiological underpinnings of the differential outcomes effect. Integr Physiol Behav Sci 36:182-195. CrossRef Medline
44. Schoenbaum G, Setlow B, Saddoris MP, Gallagher M (2003) Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39: 855-867. CrossRef Medline
45. Schoenemann PT, Sheehan MJ, Glotzer LD (2005) Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 8:242-252. CrossRef Medline
46. Semendeferi K, Lu A, Schenker N, Damasio H (2002) Humans and great apes share a large frontal cortex. Nat Neurosci 5:272-276. CrossRef Medline
47. Sescousse G, Redouté J, Dreher JC (2010) The architecture of reward value coding in the human orbitofrontal cortex. J Neurosci 30:13095-13104. CrossRef Medline
48. Simmons WK, Martin A, Barsalou LW (2005) Pictures of appetizing foods activate gustatory cortices for taste and reward. Cereb Cortex 15:1602-1608. CrossRef Medline
49. Takahashi YK, Roesch MR, Wilson RC, Toreson K, O'Donnell P, Niv Y, Schoenbaum G (2011) Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex. Nat Neurosci 14: 1590-1597. CrossRef Medline
50. Tremblay L, Schultz W (1999) Relative reward preference in primate orbitofrontal cortex. Nature 398:704-708. CrossRef Medline
51. Valentin VV, Dickinson A, O'Doherty JP (2007) Determining the neural substrates of goal-directed learning in the human brain. J Neurosci 27: 4019-4026. CrossRef Medline
52. Walton ME, Behrens TE, Buckley MJ, Rudebeck PH, Rushworth MF (2010) Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning. Neuron 65:927-939. CrossRef Medline
53. Weiskopf N, Hutton C, Josephs O, Deichmann R (2006) Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: a whole-brain analysis at 3 T and 1.5 T. Neuroimage 33:493-504. CrossRef Medline