The role of ventral frontostriatal circuitry in reward-based learning in humans

Journal of Neuroscience

Volumn 25, Issue 38, 2005, Pages 8650-8656

  Galvan, Adriana ^a,c   Hare, Todd A ^a   Davidson, Matthew ^a   Spicer, Julie ^a   Glover, Gary ^b   Casey, B J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Box 140 ^*  (United States)

Author keywords

Basal ganglia; fMRI; Learning; Nucleus accumbens; Orbital frontal cortex; Reward; Thalamocortical circuitry

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ARTICLE; BASAL GANGLION; CLINICAL ARTICLE; CORPUS STRIATUM; ELECTROPHYSIOLOGY; EVENT RELATED POTENTIAL; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LEARNING; NERVE CONDUCTION; NUCLEUS ACCUMBENS; PREDICTION; PRIORITY JOURNAL; REACTION TIME; REWARD; THALAMOCORTICAL TRACT;

ADULT; CORPUS STRIATUM; FEMALE; FRONTAL LOBE; HUMANS; LEARNING; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PSYCHOMOTOR PERFORMANCE; REACTION TIME; REWARD;

EID: 25444465628     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2431-05.2005     Document Type: Article

References (52)

1. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
2. Amso D, Davidson MC, Johnson SP, Glover G, Casey BJ (2005) Contributions of the hippocampus and the striatum to simple association and frequency-based learning. NeuroImage 27:291-298.
3. Berns GS, McClure SM, Pagnoni P, Montague PR (2001) Predictability modulates human brain response to reward. J Neurosci 21:2793-2798.
4. Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DW (2004) Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J Neurosci 24:1793-1802.
5. Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207-4221.
6. Breiter HC, Golub RL, Weisskoff RM, Kennedy DN, Makris N, Berke JD, Goodman JM, Kantor HL, Gastfriend DR, Riordan JP, Mathew RT, Rosen BR, Hyman SE (1997) Acute effects of cocaine on human brain activity and emotion. Neuron 19:591-611.
7. Cromwell HC, Schultz W (2003) Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. J Neurophysiol 89:2823-2838.
8. Dagenbach D, Kubat-Silman AK, Absher JR (2001) Human verbal working memory impairments associated with thalamic damage. Int J Neurosci 111:67-87.
9. Davidson MC, Horvitz JC, Tottenham N, Fossella JA, Watts R, Ulug AM, Casey BJ (2004) Differential cingulated and caudate activation following unexpected nonrewarding stimuli. NeuroImage 23:1039-1045.
10. Dayan P, Balleine BW (2002) Reward, motivation, and reinforcement learning. Neuron 36:285-298.
11. 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.
12. Delgado MR, Locke HM, Stenger VA, Fiez JA (2003) Dorsal striatum responses to reward and punishment: effects of valence and magnitude manipulations. Cogn Affect Behav Neurosci 3:27-38.
13. Delgado MR, Miller MM, Inati S, Phelps EA (2005) An fMRI study of reward-related probability learning. NeuroImage 24:862-873.
14. Duvernoy HM (1991) The human brain, Ed 2. New York: Springer Wien.
15. Elliott R, Newman JL, Longe OA, Deakin JF (2003) Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: a parametric functional magnetic resonance imaging study. J Neurosci 23:303-307.
16. Elliott R, Newman JL, Longe OA, William Deakin JF (2004) Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems. NeuroImage 21:984-990.
17. Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299:1898-1902.
18. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636-647.
19. Fuster J (2001) The prefrontal cortex-an update: time is of the essence. Neuron 30:319-333.
20. Glover GH, Thomason ME (2004) Improved combination of spiral-in/out images for BOLD fMRI. Magn Reson Med 51:863-868.
21. Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317-330.
22. Hollerman JR, Schultz W (1998) Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci 1:304-309.
23. Hyman SE, Malenka RC (2001) Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2:695-703.
24. Ito R, Dalley JW, Robbins TW, Everitt BJ (2002) Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J Neurosci 22:6247-6253.
25. Ito R, Robbins TW, Everitt BJ (2004) Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7:389-397.
26. Knutson B, Adams CM, Fong GW, Hommer D (2001a) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159(1-5).
27. Knutson B, Fong GW, Adams CM, Varner JL, Hommer D (2001b) Dissociation of reward anticipation and outcome with event-related fMRI. NeuroReport 12:3683-3687.
28. 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.
29. Kringelbach ML, O'Doherty J, Rolls ET, Andrews C (2003) Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with is subjective pleasantness. Cereb Cortex 13:1064-1071.
30. Kubat-Silman AK, Dagenbach D, Absher JR (2002) Patterns of impaired verbal, spatial, and object working memory after thalamic lesions. Brain Cogn 50:178-193.
31. Leon MI, Shadlen MN (1999) Effect of expected reward magnitude on the response in the dorsolateral prefrontal cortex of the macaque. Neuron 24:415-425.
32. MacDonald III AW, Cohen JD, Stenger VA, Carter CS (2000) Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288:1835-1838.
33. May JC, Delgado MR, Dahl RE, Stenger VA, Ryan ND, Fiez JA, Carter CS (2004) Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents. Biol Psychiatry 55:359-366.
34. McFarland NR, Haber SN (2002) Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 22:8117-8132.
35. Mirenowicz J, Schultz W (1994) Importance of unpredictability for reward responses in primate dopamine neurons. J Neurophysiol 72:1024-1027.
36. Montague PR, Hyman SE, Cohen JD (2004) Computational roles for dopamine in behavioral control. Nature 431:760-767.
37. O'Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G, Renner B, Ahne G (2000) Sensory-specific satiety-related olfactory activation of the human orbitofronal cortex. NeuroReport 11:893-897.
38. 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.
39. O'Doherty JP (2004) Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 14:769-776.
40. O'Doherty JP, Dayan P, Friston K, Critchley H, Dolan RJ (2003) Temporal difference models and reward-related learning in the human brain. Neuron 38:329-337.
41. Pasupathy A, Miller EK (2005) Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433:873-876.
42. Pavlov IP (1903) The experimental psychology and psychopathology of animals. Paper presented at 14th International Medical Congress, Madrid, Spain.
43. Pavlov IP (1927) Conditioned reflexes. Oxford: Oxford UP.
44. Ramnani N, Miall RC (2003) Instructed delay activity in the human prefrontal cortex is modulated by monetary reward expectation. Cereb Cortex 13:318-327.
45. Ridley RM, Baker HF, Mills DA, Green ME, Cummings RM (2004) Topographical memory impairments after unilateral lesions of the anterior thalamus and contralateral inferotemporal cortex. Neuropsychologia 42:1178-1191.
46. Robinson TE, Berridge KC (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95 [Suppl 2]:S91-S117.
47. Rolls ET, Kringelbach ML, De Araujo IE (2003) Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci 18:695-703.
48. Talairach J, Tournoux (1988) Co-planar stereotaxic atlas of the human brain. New York: Thieme.
49. Tremblay L, Schultz W (1999) Relative reward preference in primate orbitofrontal cortex. Nature 398:704-708.
50. Volkow ND, Fowler JS, Wang GJ, Swanson JM (2004) Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Mol Psychiatry 9:557-569.
51. Wallis JD, Miller EK (2003) Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18:2069-2081.
52. Wallis JD, Dias R, Robbins TW, Roberts AC (2001) Dissociable contributions of the orbitofrontal and lateral prefrontal cortex of the marmoset to performance on a detour reaching task. Eur J Neurosci 13:1797-1808.