Contrasting effects of medial and lateral orbitofrontal cortex lesions on credit assignment and decision-making in humans

Journal of Neuroscience

Volumn 37, Issue 29, 2017, Pages 7023-7035

  Noonan, Maryann P ^a,b   Chau, Bolton K H ^c   Rushworth, Matthew F S ^a   Fellows, Lesley K ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MCGILL UNIVERSITY   (Canada)

^c HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

Author keywords

Credit assignment; Decision making; Orbitofrontal cortex; Prefrontal cortex; Reward; Ventromedial prefrontal cortex

Indexed keywords

ANALYTICAL PARAMETERS; ARTICLE; BECK DEPRESSION INVENTORY; BEHAVIORAL SCIENCE; BRAIN CORTEX LESION; CLINICAL ARTICLE; CONTROLLED STUDY; CREDIT ASSIGNMENT; DECISION MAKING; FEMALE; HUMAN; LATERAL ORBITOFRONTAL CORTEX; MALE; MEDIAL ORBITOFRONTAL CORTEX; NEUROPSYCHOLOGICAL TEST; PRIORITY JOURNAL; REWARD; REWARD LEARNING; TASK PERFORMANCE; WORKING MEMORY; ADULT; BRAIN INJURY; INJURIES; MIDDLE AGED; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; REINFORCEMENT; YOUNG ADULT;

ADULT; BRAIN INJURIES; CHOICE BEHAVIOR; FEMALE; HUMANS; MALE; MIDDLE AGED; NERVE NET; PREFRONTAL CORTEX; TOKEN ECONOMY; YOUNG ADULT;

EID: 85025132401     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0692-17.2017     Document Type: Article

References (66)

1. Akaishi R, Kolling N, Brown JW, Rushworth M (2016) Neural mechanisms of credit assignment in a multicue environment. J Neurosci 36:1096– 1112. CrossRef Medline
2. Barraclough DJ, Conroy ML, Lee D (2004) Prefrontal cortex and decision-making in a mixed-strategy game. Nat Neurosci 7:404–410. 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. 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
5. Camille N, Griffiths CA, Vo K, Fellows LK, Kable JW (2011) Ventromedial frontal lobe damage disrupts value maximization in humans. J Neurosci 31:7527–7532. CrossRef Medline
6. Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346: 366–402. CrossRef Medline
7. Carmichael ST, Price JL (1995a) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641. CrossRef Medline
8. Carmichael ST, Price JL (1995b) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642–664. 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. Chau BK, Kolling N, Hunt LT, Walton ME, Rushworth MF (2014) A neural mechanism underlying failure of optimal choice with multiple alternatives. Nat Neurosci 17:463–470. CrossRef Medline
11. Chau BK, Sallet J, Papageorgiou GK, Noonan MP, Bell AH, Walton ME, Rushworth MF (2015) Contrasting roles for orbitofrontal cortex and amygdala in credit assignment and learning in macaques. Neuron 87: 1106–1118. CrossRef Medline
12. Cisek P (2012) Making decisions through a distributed consensus. Curr Opin Neurobiol 22:927–936. CrossRef Medline
13. Clark L, Bechara A, Damasio H, Aitken MR, Sahakian BJ, Robbins TW (2008) Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making. Brain 131:1311–1322. CrossRef Medline
14. Damasio AR (1994) Descartes’ error: emotion, reason, and the human brain. New York: Putnam.
15. Economides M, Guitart-Masip M, Kurth-Nelson Z, Dolan RJ (2014) Anterior cingulate cortex instigates adaptive switches in choice by integrating immediate and delayed components of value in ventromedial prefrontal cortex. J Neurosci 34:3340–3349. CrossRef Medline
16. Fellows LK (2006) Deciding how to decide: ventromedial frontal lobe damage affects information acquisition in multi-attribute decision-making. Brain 129:944–952. CrossRef Medline
17. Fellows LK, Farah MJ (2003) Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. Brain 126:1830–1837. CrossRef Medline
18. Fellows LK, Farah MJ (2005) Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. Cereb Cortex 15:58–63. CrossRef Medline
19. Fellows LK, Farah MJ (2007) The role of ventromedial prefrontal cortex in decision-making: judgment under uncertainty or judgment per se? Cereb Cortex 17:2669–2674. CrossRef Medline
20. Gottlieb J, Hayhoe M, Hikosaka O, Rangel A (2014) Attention, reward, and information seeking. J Neurosci 34:15497–15504. CrossRef Medline
21. Henri-Bhargava A, Simioni A, Fellows LK (2012) Ventromedial frontal lobe damage disrupts the accuracy, but not the speed, of value-based preference judgments. Neuropsychologia 50:1536–1542. CrossRef Medline
22. Hornak J, O’Doherty J, Bramham J, Rolls ET, Morris RG, Bullock PR, Polkey CE (2004) Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J Cogn Neurosci 16:463–478. CrossRef Medline
23. Howard JD, Gottfried JA, Tobler PN, Kahnt T (2015) Identity-specific coding of future rewards in the human orbitofrontal cortex. Proc Natl Acad Sci U S A 112:5195–5200. CrossRef Medline
24. Howard JD, Kahnt T, Gottfried JA (2016) Converging prefrontal pathways support associative and perceptual features of conditioned stimuli. Nat Commun 7:11546. CrossRef Medline
25. Hunt LT, Hayden BY (2017) A distributed, hierarchical and recurrent framework for reward-based choice. Nat Rev Neurosci 18:172–182. CrossRef Medline
26. Hunt LT, Behrens TE, Hosokawa T, Wallis JD, Kennerley SW (2015) Capturing the temporal evolution of choice across prefrontal cortex. eLife 4:e11945. CrossRef Medline
27. Jocham G, Hunt LT, Near J, Behrens TE (2012) A mechanism for value-guided choice based on the excitation-inhibition balance in prefrontal cortex. Nat Neurosci 15:960–961. CrossRef Medline
28. Jocham G, Brodersen KH, Constantinescu AO, Kahn MC, Ianni AM, Walton ME, Rushworth MF, Behrens TE (2016) Reward-guided learning with and without causal attribution. Neuron 90:177–190. CrossRef Medline
29. Kahnt T, Chang LJ, Park SQ, Heinzle J, Haynes JD (2012) Connectivity-based parcellation of the human orbitofrontal cortex. J Neurosci 32: 6240–6250. CrossRef Medline
30. Kolling N, Behrens TE, Mars RB, Rushworth MF (2012) Neural mechanisms of foraging. Science 336:95–98. CrossRef Medline
31. Kolling N, Behrens T, Wittmann MK, Rushworth M (2016a) Multiple signals in anterior cingulate cortex. Curr Opin Neurobiol 37:36–43. CrossRef Medline
32. Kolling N, Wittmann MK, Behrens TE, Boorman ED, Mars RB, Rushworth MF (2016b) Value, search, persistence and model updating in anterior cingulate cortex. Nat Neurosci 19:1280–1285. CrossRef Medline
33. Kondo H, Saleem KS, Price JL (2005) Differential connections of the perirhinal and parahippocampal cortex with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol 493:479–509. CrossRef Medline
34. Kumaran D, Warren DE, Tranel D (2015) Damage to the ventromedial prefrontal cortex impairs learning from observed outcomes. Cereb Cortex 25:4504–4518. CrossRef Medline
35. Lau B, Glimcher PW (2007) Action and outcome encoding in the primate caudate nucleus. J Neurosci 27:14502–14514. CrossRef Medline
36. Levy DJ, Glimcher PW (2012) The root of all value: a neural common currency for choice. Curr Opin Neurobiol 22:1027–1038. CrossRef Medline
37. Lim SL, O’Doherty JP, Rangel A (2011) The decision value computations in the vmPFC and striatum use a relative value code that is guided by visual attention. J Neurosci 31:13214–13223. CrossRef Medline
38. Louie K, Grattan LE, Glimcher PW (2011) Reward value-based gain control: divisive normalization in parietal cortex. J Neurosci 31:10627–10639. CrossRef Medline
39. Luce RD (1959) Individual choice behaviour: a theoretical analysis. New York: Wiley.
40. Mackey S, Petrides M (2010) Quantitative demonstration of comparable architectonic areas within the ventromedial and lateral orbital frontal cortex in the human and the macaque monkey brains. Eur J Neurosci 32:1940–1950. CrossRef Medline
41. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699. CrossRef Medline
42. Neubert FX, Mars RB, Thomas AG, Sallet J, Rushworth MF (2014) Comparison of human ventral frontal cortex areas for cognitive control and language with areas in monkey frontal cortex. Neuron 81:700–713. CrossRef Medline
43. Neubert FX, Mars RB, Sallet J, Rushworth MF (2015) Connectivity reveals relationship of brain areas for reward-guided learning and decision-making in human and monkey frontal cortex. Proc Natl Acad Sci U S A 112:E2695–E2704. CrossRef Medline
44. 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
45. 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
46. Ongür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219. CrossRef Medline
47. 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
48. Ray P (1973) Independence of irrelevant alternatives. Econometrica 41: 987–991. CrossRef
49. Rolls ET, Hornak J, Wade D, McGrath J (1994) Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol Neurosurg Psychiatry 57:1518–1524. CrossRef Medline
50. Rudebeck PH, Murray EA (2014) The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron 84:1143–1156. CrossRef Medline
51. Rudebeck PH, Saunders RC, Prescott AT, Chau LS, Murray EA (2013) Prefrontal mechanisms of behavioral flexibility, emotion regulation and value updating. Nat Neurosci 16:1140–1145. CrossRef Medline
52. 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
53. Rushworth MF, Kolling N, Sallet J, Mars RB (2012) Valuation and decision-making in frontal cortex: one or many serial or parallel systems? Curr Opin Neurobiol 22:946–955. CrossRef Medline
54. Schmahmann JD. and Pandya DN (2006) Fiber pathways of the brain. New York: Oxford.
55. Schoenbaum G, Takahashi Y, Liu TL, McDannald MA (2011) Does the or- bitofrontal cortex signal value? Ann N Y Acad Sci 1239:87–99. CrossRef Medline
56. Seo H, Cai X, Donahue CH, Lee D (2014) Neural correlates of strategic reasoning during competitive games. Science 346:340–343. CrossRef Medline
57. Stalnaker TA, Cooch NK, Schoenbaum G (2015) What the orbitofrontal cortex does not do. Nat Neurosci 18:620–627. CrossRef Medline
58. Sul JH, Kim H, Huh N, Lee D, Jung MW (2010) Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision-making. Neuron 66:449–460. CrossRef Medline
59. Thorndike EL (1933a) A proof of the Law of Effect. Science 77:173–175. CrossRef Medline
60. Thorndike EL (1933b) The “spread” or “scatter” of the influence from a reward, in relation to Gestalt doctrines. Science 77:368. CrossRef Medline
61. Tsuchida A, Doll BB, Fellows LK (2010) Beyond reversal: a critical role for human orbitofrontal cortex in flexible learning from probabilistic feedback. J Neurosci 30:16868–16875. CrossRef Medline
62. Tsujimoto S, Genovesio A, Wise SP (2009) Monkey orbitofrontal cortex encodes response choices near feedback time. J Neurosci 29:2569–2574. CrossRef Medline
63. Vaidya AR, Fellows LK (2015) Ventromedial frontal cortex is critical for guiding attention to reward-predictive visual features in humans. J Neurosci 35:12813–12823. CrossRef Medline
64. Vaidya AR, Fellows LK (2016) Necessary contributions of human frontal lobe subregions to reward learning in a dynamic, multidimensional environment. J Neurosci 36:9843–9858. CrossRef Medline
65. 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
66. Zald DH, McHugo M, Ray KL, Glahn DC, Eickhoff SB, Laird AR (2014) Meta-analytic connectivity modeling reveals differential functional connectivity of the medial and lateral orbitofrontal cortex. Cereb Cortex 24:232–248. CrossRef Medline