title: Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks.
abstract: Here we challenge the view that reward-guided learning is solely controlled by the mesoaccumbens pathway arising from dopaminergic neurons in the ventral tegmental area and projecting to the nucleus accumbens. This widely accepted view assumes that reward is a monolithic concept, but recent work has suggested otherwise. It now appears that, in reward-guided learning, the functions of ventral and dorsal striata, and the cortico-basal ganglia circuitry associated with them, can be dissociated. Whereas the nucleus accumbens is necessary for the acquisition and expression of certain appetitive Pavlovian responses and contributes to the motivational control of instrumental performance, the dorsal striatum is necessary for the acquisition and expression of instrumental actions. Such findings suggest the existence of multiple independent yet interacting functional systems that are implemented in iterating and hierarchically organized cortico-basal ganglia networks engaged in appetitive behaviors ranging from Pavlovian approach responses to goal-directed instrumental actions controlled by action-outcome contingencies.
authors.affiliation: Department of Psychology and Neuroscience, Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA. hy43@duke.edu
authors.forename: Henry H
authors.initials: HH
authors.lastname: Yin
authors.forename: Sean B
authors.initials: SB
authors.lastname: Ostlund
authors.forename: Bernard W
authors.initials: BW
authors.lastname: Balleine
mesh_terms: D000818:Animals; D002540:Cerebral Cortex / Q000033:anatomy & histology / Q000502:physiology*; D003213:Conditioning, Psychological / Q000502:physiology; D004298:Dopamine / Q000502:physiology*; D006801:Humans; D007858:Learning / Q000502:physiology*; D017072:Neostriatum / Q000033:anatomy & histology / Q000502:physiology*; D009434:Neural Pathways / Q000033:anatomy & histology / Q000502:physiology; D009714:Nucleus Accumbens / Q000033:anatomy & histology / Q000502:physiology*; D012201:Reward; D017557:Ventral Tegmental Area / Q000502:physiology; D014836:Volition / Q000502:physiology
chemical_list: D004298:Dopamine
references.citation: J Neurosci. 2000 Oct 15;20(20):7737-42
references.pmid: 11027236
references.citation: Neuron. 2008 Feb 7;57(3):432-41
references.pmid: 18255035
references.citation: Behav Neurosci. 2000 Jun;114(3):468-83
references.pmid: 10883798
references.citation: Trends Neurosci. 2006 May;29(5):272-9
references.pmid: 16545468
references.citation: Neurobiol Learn Mem. 2006 May;85(3):283-8
references.pmid: 16423542
references.citation: Eur J Neurosci. 2007 Apr;25(8):2491-7
references.pmid: 17445244
references.citation: J Neurosci. 2003 Nov 12;23(32):10402-10
references.pmid: 14614099
references.citation: Neuron. 2000 Mar;25(3):515-32
references.pmid: 10774721
references.citation: Eur J Neurosci. 2005 Jul;22(2):513-23
references.pmid: 16045504
references.citation: Exp Brain Res. 2002 Sep;146(1):122-6
references.pmid: 12192586
references.citation: J Neurophysiol. 2006 Feb;95(2):948-59
references.pmid: 16192338
references.citation: Nat Neurosci. 1998 Sep;1(5):411-6
references.pmid: 10196532
references.citation: Eur J Neurosci. 2004 Jan;19(1):181-9
references.pmid: 14750976
references.citation: Annu Rev Neurosci. 1988;11:329-52
references.pmid: 3284445
references.citation: J Neurophysiol. 1989 Apr;61(4):814-32
references.pmid: 2723722
references.citation: Ann N Y Acad Sci. 2007 May;1104:192-212
references.pmid: 17416920
references.citation: Eur J Neurosci. 2005 Jul;22(2):505-12
references.pmid: 16045503
references.citation: Science. 1964 Nov 20;146(3647):1071-2
references.pmid: 14202465
references.citation: Neuron. 2005 Feb 17;45(4):587-97
references.pmid: 15721244
references.citation: J Neurosci. 2006 Jan 4;26(1):217-22
references.pmid: 16399690
references.citation: J Neurosci. 1999 Dec 1;19(23):10502-11
references.pmid: 10575046
references.citation: Nat Neurosci. 2005 Jun;8(6):805-12
references.pmid: 15908948
references.citation: J Neurophysiol. 1998 Jul;80(1):1-27
references.pmid: 9658025
references.citation: Science. 2004 Apr 16;304(5669):452-4
references.pmid: 15087550
references.citation: J Neurosci. 2000 Nov 1;20(21):8122-30
references.pmid: 11050134
references.citation: Physiol Behav. 2005 Dec 15;86(5):717-30
references.pmid: 16257019
references.citation: BMC Neurosci. 2005 Feb 03;6:9
references.pmid: 15691387
references.citation: J Exp Psychol Anim Behav Process. 1983 Jul;9(3):225-47
references.pmid: 6153052
references.citation: Psychol Rev. 1957 Jul;64(4):217-28
references.pmid: 13453606
references.citation: Annu Rev Neurosci. 2006;29:565-98
references.pmid: 16776597
references.citation: Learn Mem. 2004 Jul-Aug;11(4):459-63
references.pmid: 15286184
references.citation: Exp Brain Res. 1997 Jun;115(1):1-5
references.pmid: 9224828
references.citation: Science. 2005 Nov 25;310(5752):1337-40
references.pmid: 16311337
references.citation: Brain Res Brain Res Rev. 1998 Dec;28(3):309-69
references.pmid: 9858756
references.citation: J Neurophysiol. 1997 Mar;77(3):1313-24
references.pmid: 9084599
references.citation: Proc Natl Acad Sci U S A. 2005 Apr 26;102(17):6189-94
references.pmid: 15833811
references.citation: Nat Neurosci. 2004 Jun;7(6):583-4
references.pmid: 15146188
references.citation: Learn Mem. 2006 Mar-Apr;13(2):123-6
references.pmid: 16547159
references.citation: Neural Netw. 2002 Jun-Jul;15(4-6):507-21
references.pmid: 12371508
references.citation: Neuroscience. 2000;96(3):451-74
references.pmid: 10717427
references.citation: J Neurophysiol. 1998 Aug;80(2):947-63
references.pmid: 9705481
references.citation: Eur J Neurosci. 2003 Sep;18(5):1286-94
references.pmid: 12956727
references.citation: Adv Pharmacol. 1998;42:686-90
references.pmid: 9327992
references.citation: Behav Brain Res. 2002 Dec 2;137(1-2):149-63
references.pmid: 12445721
references.citation: Neuron. 2007 Apr 19;54(2):237-44
references.pmid: 17442245
references.citation: J Chem Neuroanat. 2003 Dec;26(4):317-30
references.pmid: 14729134
references.citation: Neurosci Biobehav Rev. 2006;30(2):148-72
references.pmid: 16125239
references.citation: Neuroimage. 2005 Feb 1;24(3):862-73
references.pmid: 15652321
references.citation: J Neurosci. 2001 May 1;21(9):3251-60
references.pmid: 11312310
references.citation: Q J Exp Psychol B. 1990 Feb;42(1):59-71
references.pmid: 2326494
references.citation: Nature. 2004 Oct 14;431(7010):760-7
references.pmid: 15483596
references.citation: J Exp Anal Behav. 1968 Jan;11(1):1-8
references.pmid: 5636851
references.citation: J Exp Anal Behav. 1980 Nov;34(3):297-304
references.pmid: 16812191
references.citation: Adv Neurol. 1993;60:62-70
references.pmid: 8380529
references.citation: Behav Brain Res. 2006 Jan 30;166(2):189-96
references.pmid: 16153716
references.citation: Trends Neurosci. 2007 May;30(5):220-7
references.pmid: 17400299
references.citation: Q J Exp Psychol B. 1996 Nov;49(4):289-306
references.pmid: 8962537
references.citation: J Comp Physiol Psychol. 1968 Aug;66(1):1-5
references.pmid: 5672628
references.citation: Proc Natl Acad Sci U S A. 2007 May 29;104(22):9493-8
references.pmid: 17519340
references.citation: Nat Neurosci. 2002 Dec;5(12):1327-31
references.pmid: 12426572
references.citation: J Exp Anal Behav. 1969 Jul;12(4):511-20
references.pmid: 16811370
references.citation: Nat Neurosci. 2007 Jan;10(1):15-7
references.pmid: 17189947
references.citation: Neural Netw. 2006 Oct;19(8):1242-54
references.pmid: 16987637
references.citation: Psychol Rev. 1967 May;74(3):151-82
references.pmid: 5342881
references.citation: Brain Res. 2000 Dec 15;886(1-2):113-164
references.pmid: 11119693
references.citation: J Neurosci. 2000 Mar 15;20(6):2369-82
references.pmid: 10704511
references.citation: Neuron. 2006 Sep 7;51(5):541-7
references.pmid: 16950153
references.citation: Learn Mem. 2005 May-Jun;12(3):285-95
references.pmid: 15930507
references.citation: Neuropharmacology. 1998 Apr-May;37(4-5):407-19
references.pmid: 9704982
references.citation: Neuroscientist. 2006 Dec;12(6):500-11
references.pmid: 17079516
references.citation: Nat Neurosci. 2007 Jan;10(1):126-31
references.pmid: 17187065
references.citation: Eur J Neurosci. 2005 Nov;22(10):2605-16
references.pmid: 16307603
references.citation: J Neurosci. 2005 Mar 16;25(11):2771-80
references.pmid: 15772337
references.citation: Annu Rev Neurosci. 2001;24:167-202
references.pmid: 11283309
references.citation: Psychopharmacology (Berl). 2007 Apr;191(3):507-20
references.pmid: 17031711
references.citation: J Neurosci. 2001 Dec 1;21(23):9471-7
references.pmid: 11717381
references.citation: J Neurosci. 2011 Aug 17;31(33):11786-94
references.pmid: 21849539
references.citation: Neuroscientist. 2007 Apr;13(2):148-59
references.pmid: 17404375
references.citation: Neurosci Biobehav Rev. 2002 May;26(3):321-52
references.pmid: 12034134
references.citation: J Neurophysiol. 2007 Feb;97(2):1621-32
references.pmid: 17122317
references.citation: J Neurophysiol. 1997 Mar;77(3):1325-37
references.pmid: 9084600
references.citation: J Neurosci. 2008 Apr 23;28(17):4398-405
references.pmid: 18434518
references.citation: Science. 2003 Mar 21;299(5614):1898-902
references.pmid: 12649484
references.citation: Neuron. 2004 Jan 22;41(2):281-92
references.pmid: 14741108
references.citation: J Neurosci. 2004 Feb 18;24(7):1660-5
references.pmid: 14973239
references.citation: Psychopharmacology (Berl). 2007 Apr;191(3):567-78
references.pmid: 17093978
references.citation: Nat Neurosci. 2005 Nov;8(11):1481-9
references.pmid: 16251991
references.citation: Eur J Neurosci. 2007 Dec;26(11):3141-9
references.pmid: 18005062
references.citation: Neuroscience. 1994 Nov;63(2):363-79
references.pmid: 7891852
references.citation: Behav Neurosci. 2000 Feb;114(1):42-63
references.pmid: 10718261
references.citation: Life Sci. 1989;45(21):1943-57
references.pmid: 2689823
references.citation: J Neurosci. 2005 Feb 2;25(5):1193-202
references.pmid: 15689556
references.citation: Curr Biol. 2004 Jul 13;14(13):1124-34
references.pmid: 15242609
references.citation: J Exp Anal Behav. 1971 Mar;15(2):237-41
references.pmid: 16811508
references.citation: Nature. 2001 Jul 5;412(6842):43-8
references.pmid: 11452299
references.citation: Behav Brain Res. 2003 Nov 30;146(1-2):145-57
references.pmid: 14643467
references.citation: Cereb Cortex. 2004 Sep;14(9):1022-30
references.pmid: 15115748
references.citation: Adv Neurol. 1993;60:107-12
references.pmid: 8093572
references.citation: Brain Res Rev. 2008 Aug;58(2):303-13
references.pmid: 18433875
references.citation: J Neurophysiol. 1992 Jan;67(1):145-63
references.pmid: 1552316
references.citation: Neuroscience. 1978;3(4-5):385-401
references.pmid: 683502
references.citation: J Neurosci. 2007 Dec 19;27(51):13977-81
references.pmid: 18094235
references.citation: Neuron. 2002 Oct 10;36(2):285-98
references.pmid: 12383782
references.citation: J Neurophysiol. 2006 Jan;95(1):301-10
references.pmid: 16192329
references.citation: Science. 1997 Mar 14;275(5306):1593-9
references.pmid: 9054347
references.citation: Nat Neurosci. 2006 Aug;9(8):1057-63
references.pmid: 16862149
references.citation: Nat Neurosci. 2007 Aug;10(8):1020-8
references.pmid: 17603481
references.citation: J Neurosci. 2002 Jul 1;22(13):5705-12
references.pmid: 12097522
references.citation: J Exp Psychol Anim Behav Process. 1975 Oct;1(4):355-63
references.pmid: 1202141
references.citation: Annu Rev Neurosci. 1986;9:357-81
references.pmid: 3085570
references.citation: Neurosci Biobehav Rev. 2000 Jan;24(1):85-105
references.pmid: 10654664
references.citation: Brain Res. 2005 Nov 9;1061(2):88-96
references.pmid: 16226228
references.citation: J Exp Psychol Anim Behav Process. 2004 Apr;30(2):104-17
references.pmid: 15078120
references.citation: Eur J Neurosci. 2006 Mar;23(5):1341-51
references.pmid: 16553795
references.citation: Eur J Neurosci. 2007 Feb;25(3):847-53
references.pmid: 17328779
references.citation: Prog Brain Res. 1990;85:95-116; discussion 116-8
references.pmid: 2094917
references.citation: Proc Natl Acad Sci U S A. 2004 Sep 7;101(36):13124-31
references.pmid: 15331782
references.citation: Behav Neurosci. 2002 Feb;116(1):174-7
references.pmid: 11895179