Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition

Biological Psychiatry

Volumn 55, Issue 6, 2004, Pages 594-602

  Rogers, Robert D ^a   Ramnani, Narender ^b   Mackay, Clare ^a   Wilson, James L ^b   Jezzard, Peter ^b   Carter, Cameron S ^c   Smith, Stephen M ^b  

^a WARNEFORD HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Anterior cingulate; Decision making; Emotion; Functional magnetic resonance imaging; Orbitofrontal; Reward

Indexed keywords

ADULT; ARTICLE; BLOOD OXYGENATION; CINGULATE GYRUS; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; EVENT RELATED POTENTIAL; HUMAN; HUMAN EXPERIMENT; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ORBITAL CORTEX; OUTCOMES RESEARCH; PREFRONTAL CORTEX; PRIORITY JOURNAL; REWARD; VOLUNTEER;

ADULT; BRAIN MAPPING; CHOICE BEHAVIOR; DECISION MAKING; ECHO-PLANAR IMAGING; FEMALE; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PREFRONTAL CORTEX; PROBABILITY; REWARD; TIME FACTORS;

EID: 1542375848     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2003.11.012     Document Type: Article

References (72)

1. Barbas H., Pandya D.N. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol. 286:1989;353-375.
2. Bechara A., Tranel D., Damasio H., Damasio A.R. Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cereb Cortex. 6:1996;215-225.
3. Bechara A., Damasio H., Tranel D., Anderson S.W. Dissociation of working memory from decision making within the human prefrontal cortex. J Neurosci. 19:1998;5473.
4. Berns G.S., McGlure S.M., Pagnoni G., Montague P.R. Predictability modulates human brain response to reward. J Neurosci. 21:2001;2793-2798. 54s81.
5. Botnivick M.M., Braver T.S., Barch D.M., Carter C.S., Cohen J.D. Conflict monitoring and cognitive control. Psychol Rev. 108:2001;624-652.
6. Breiter H.C., Aharon I., Kahneman D., Dale A., Shizgal P. Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron. 30:2001;619-639.
7. Breiter H.C., Gollub R.L., Weisskoff R.M., Kennedy D.N., Makris N., Berke J.D., et al. Acute effects of cocaine on human brain activity and emotion. Neuron. 19:1997;591-611.
8. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 4:2000;215-222.
9. Bush G., Vogt B.A., Holmes J., Dale A.M., Greve D., Jenicke M.A., Rosen B.R. Dorsal anterior cingulate cortex A role in reward-based decision making. Proc Natl Acad Sci U S A. 9:2002;523-528.
10. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation The role of the amygdala, ventral striatum and prefrontal cortex. Neurosci Biobehav Rev. 26:2002;321-352.
11. Carmichael S.T., Price J.L. Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol. 371:1996;179-207.
12. Castelli F., Happe F., Frith U., Frith C.D. Movement and mind A functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage. 12:2000;314-325.
13. Critchley H.D., Elliott R., Mathias C.J., Dolan R.J. Neural activity relating to generation and representation of galvanic skin conductance responses A functional magnetic resonance imaging study. J Neurosci. 20:2000;3033-3040.
14. Damasio A.R. Descartes' Error. 1994;Grosset/Pullman, New York.
15. Delgado M.R., Nystrom L.E., Fissell C., Noll D.C., Fiez J.A. Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol. 84:2000;3072-3077.
16. Devinsky O., Morrell M.J., Vogt B.A. Contributions of anterior cingulate cortex to behaviour. Brain. 118:1995;279-306.
17. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders. Nature. 386:1997;824-827.
18. Elliot R., Rees G., Dolan R.J. Ventromedial prefrontal cortex mediates guessing. Neuropsychologia. 37:1999;403-411.
19. Elliot R., Friston K.J., Dolan R.J. Dissociable neural responses in human reward systems. J Neurosci. 20:2000;6159-6165.
20. Elliot R., Newman R.L., Longe O.A., Deakin J.F.W. Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans A parametric functional magnetic resonance imaging study. J Neurosci. 23:2003;303-307.
21. Ernst M., Bolla K., Mouratidis M., Contoreggi C., Matochik J.A., Kurian V., et al. Decision-making in a risk-taking task A PET study. Neuropsychopharmacology. 26:2002;682-691.
22. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintun M.A., Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI) Use of a cluster-size threshold. Magn Reson Med. 33:1995;636-647.
23. Francis S., Rolls E.T., Bowtell R., McGlone F., O'Doherty J., Browning A., Clare S., Smith E. The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport. 10:1999;453-459.
24. Friston K.J., Worsley K.J., Frakowiak R.S.J., Mazziotta J.C., Evans A.C. Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp. 1:1994;214-220.
25. Gallagher M., McMahan R.W., Schoenbaum G. Orbitofrontal cortex and representation of incentive value in associative learning. J Neurosci. 19:1999;6610-6614.
26. Gusnard D.A., Akbudak E., Shulman G.L., Raichle M.E. Medial prefrontal cortex and self-referential mental activity Relation to a default mode of brain function. Proc Natl Acad Sci U S A. 98:2001;4259-4264.
27. Hadland K.A., Rushworth M.F.S., Gaffan D., Passingham R.E. The anterior cingulate and reward-guided selection of actions. J Neurophysiol. 89:2003;1161-1164.
28. Howell D.C. Statistical Methods for Psychology. 1987;PWS Publishers, Boston.
29. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 17:2002;825-841.
30. Kahneman D., Tversky A. Prospect theory An analysis of decision under risk. Econometrica. 47:1979;263-291.
31. Knutson B., Adams C.M., Fong G.W., Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci. 21:2001;RC159.
32. Knutson B., Fong G.W., Adams C.M., Varner J.L., Hommer D. Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport. 12:2001;3683-3687.
33. Knutson B., Fong G.W., Bennett S.M., Adams C.M., Hommer D. A region of mesial prefrontal cortex tracks monetarily rewarding outcomes Characterization with rapid event-related fMRI. Neuroimage. 18:2003;263-272.
34. Koski L., Paus T. Functional connectivity of the anterior cingulate cortex within the human frontal lobe A brain-mapping meta-analysis. Exp Brain Res. 133:2000;55-65.
35. Lane R.D., Reiman E.M., Ahern G.L., Schwartz G.E., Davidson R.J. Neuroanatomical correlates of happiness, sadness, and disgust. Am J Psychiatry. 154:1997;926-933.
36. Lane R.D., Reiman E.M., Bradley M.M., Lang P.J., Ahern G.L., Davidson R.J., Schwartz G.E. Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia. 35:1997;1437-1444.
37. Lewinsohn P.M., Graf M. Pleasant activities and depression. J Consult Clin Psychol. 41:1973;261-268.
38. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action Functional interface between the limbic system and the motor system. Prog Neurobiol. 14:1980;69-97.
39. O'Doherty J., Critchley H., Deichmann R., Dolan R.J. Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortex. J Neurosci. 23:2003;7931-7939.
40. O'Doherty J., Kringelbach M.L., Rolls E.T., Hornak J., Andrews C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci. 4:2001;95-102.
41. O'Doherty J., Rolls E.T., Francis S., Bowtell R., McGlone F. Representation of pleasant, aversive taste in the human brain. J Neurophysiol. 85:2001;1315-1321.
42. Ojemann J.G., Akbudak E., Snyder A.Z., McKinstry R.C., Raichle M.E., Conturo T.E. Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. Neuroimage. 6:1997;156-167.
43. Ongur D., Ferry A.T., Price J.L. Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol. 460:2003;425-449.
44. Ongur D., Price J.L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex. 10:2000;206-219.
45. Parkinson J.A., Dalley J.W., Bamford A., Fehnert B., Robbins T.W. Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behaviour Further evidence for limbic cortico-ventral striatopallidal systems. Behav Neurosci. 114:2000;42-63.
46. Patterson J.C., Ungerleider L.G., Bandettini P.A. Task-independent functional brain activity correlation with skin conductance changes An fMRI study. Neuroimage. 17:2002;1797-1806.
47. Paulus M.P., Hozack N., Frank L., Brown G.G. Error rate and outcome predictability affect neural activation in prefrontal cortex and anterior cingulate during decision-making. Neuroimage. 15:(4):2002;836-846.
48. Paulus M.P., Hozack N., Zauscher B., McDowell J.E., Frank L., Brown G.G. Prefrontal, parietal, and temporal cortex networks underlie decision-making in the presence of uncertainty. Neuroimage. 13:2001;91-100.
49. Paus T., Koski L., Caramanos Z., Westbury C. Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex A review of 107 PET activation studies. Neuroreport. 9:1998;R37-R47.
50. Phan K.L., Taylor S.F., Welsh R.C., Decker L.R., Noll D.C., Nichols T.E., et al. Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal A fMRI study. Biol Psychiatry. 53:2003;211-215.
51. Phan K.L., Wager T., Taylor S.F., Liberzon I. Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal A fMRI study. Neuroimage. 16:2002;331-348.
52. Picard N., Strick P.L. Motor areas of the medial wall A review of their location and functional activation. Cereb Cortex. 6:1996;342-353.
53. Phillips M.L., Bullmore E.T., Howard R., Woodruff P.W.R., Wright I.C., Williams S.C.R., et al. Investigation of facial recognition memory and happy and sad facial expression perception An fMRI study. Psychiatry Res. 83:1998;127-138.
54. Ramnani N., Miall R.C. Instructed delay activity in the human prefrontal cortex is modulated by monetary reward expectation. Cereb Cortex. 13:2003;1-10.
55. Rogers R.D., Everitt B.J., Baldacchino A., Blackmore A.J., Swainson R., Wynne K., et al. Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers Evidence for monoaminergic mechanisms. Neuropsychopharmacology. 20:1999;322-329.
56. Rogers R.D., Owen A.M., Middleton H.C., Pickard J., Robbins T.W. Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J Neurosci. 20:1999;9029-9038.
57. Rogers R.D., Tunbridge E.M., Bhagwagar Z., Drevets W., Sahakian B.J., Carter C.S. Tryptophan depletion alters the decision-making of healthy volunteers through altered processing of reward cues. Neuropsychopharmacology. 28:2003;153-162.
58. Shidura M., Richmond B.J. Anterior cingulate Single neuronal signals related to degree of reward expectancy. Science. 296:2002;1709-1711.
59. Shima K., Tanji J. Role for cingulate motor area cells in voluntary movement selection based on reward. Science. 282:1998;1335-1338.
60. Taylor S.F., Phan K.L., Decker L.R., Liberzon I. Subjective rating of emotionally salient stimuli modulates neural activity. Neuroimage. 18:2003;650-659.
61. Teasdale J.D., Howard R.J., Cox S.G., Ha Y., Brammer M.J., Williams S.C.R., Checkley S.A. Functional MRI study of the cognitive generation of affect. Am J Psychiatry. 156:1999;209-215.
62. Thut G., Schultz W., Roelcke U., Nienhusmeier M., Missimer J., Maguire R.P., Leenders K.L. Activation of the human brain by monetary reward. Neuroreport. 8:1997;1225-1228.
63. Tranel D., Bechara A., Denburg N.L. Asymmetric functional roles of right and left ventromedial prefrontal cortices in social conduct, decision-making, and emotional processing. Cortex. 38:2002;589.
64. Tremblay L., Schultz W. Relative reward preference in primate orbitofrontal cortex. Nature. 398:1999;704-708. 612.
65. van Veen V., Cohen J.D., Botnivick M.M., Stenger V.A., Carter C.S. Anterior cingulate cortex, conflict monitoring and levels of processing. Neuroimage. 14:2001;1302-1308.
66. Vogt B.A., Nimchinsky E.A., Vogt L.J., Hof P.R. Human cingulate cortex Surface features, flat maps, and cytoarchitecture. J Comp Neurol. 359:1995;490-506.
67. Walton M.E., Bannerman D.M., Rushworth M.F. The role of rat medial frontal cortex in effort-based decision making. J Neurosci. 22:2002;10996-11003.
68. Whalen P.J., Bush G., McNally R.J., Wilhelm S., McInerney S.C., Jenicke M.A., Rauch S.L. The emotional counting Stroop paradigm A functional magnetic resonance imaging probe of the anterior cingulate affective division. Biol Psychiatry. 44:1998;1219-1228.
69. Wilson J.L., Jenkinson M., de Araujo I., Kringelbach M.L., Rolls E.T., Jezzard P. Fast, fully automated global and local magnetic field optimization for fMRI of the human brain. Neuroimage. 17:2002;967-976.
70. Woolrich M, Behrens T, Bechmann C, Jenkinson M, Smith S.(in press): Multi-level linear modeling for fMRI group analysis using Bayesian inference. Neuroimage.
71. Woolrich M.W., Ripley B.D., Brady M., Smith S.M. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage. 14:2001;1370-1386.
72. Worsley K.J., Evans A.C., Marrett S., Neelin P. A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab. 12:1992;900-918.