The role of the basal ganglia in motivated Behaviour

Reviews in the Neurosciences

Volumn 23, Issue 5-6, 2012, Pages 747-767

  Da Cunha, Claudio ^a   Gomez A, Alexander ^a   Blaha, Charles D ^b  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b University of Memphis   (United States)

Author keywords

Action selection; Basal ganglia; Decisionmaking; Dopamine; Motivated behavior; Motivation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; DOPAMINE;

ADAPTIVE BEHAVIOR; ANTERIOR CINGULATE; ANXIETY; ARTICLE; BASAL GANGLION; BEHAVIOR CHANGE; BEHAVIOR THEORY; BEHAVIORAL SCIENCE; BRAIN FUNCTION; COGNITION; CORPUS STRIATUM; DEFENSIVE BEHAVIOR; DISTRESS SYNDROME; DOPAMINERGIC NERVE CELL; EPISODIC MEMORY; EVOKED MUSCLE RESPONSE; EXECUTIVE FUNCTION; EXTRACELLULAR SPACE; HABIT; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS; INTRACELLULAR SIGNALING; LEARNING; MAJOR DEPRESSION; MESENCEPHALON; MOTIVATION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY BULB; ORBITAL CORTEX; PRIORITY JOURNAL; SEMANTIC MEMORY; SIGNAL NOISE RATIO; STIMULUS RESPONSE; SUBSTANTIA NIGRA PARS COMPACTA; THALAMUS; VENTRAL TEGMENTUM; VOCALIZATION;

ANIMALS; BASAL GANGLIA; CONDITIONING, CLASSICAL; HUMANS; MOTIVATION;

EID: 84869403445     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/revneuro-2012-0063     Document Type: Article

References (235)

1. Aggleton, J.P. and Brown, M.W. (1999). Episodic memory, amnesia and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 22, 425-444.
2. Albin, R.L., Young, A.B., and Penney, J.B. (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375.
3. Alcaro, A. and Panksepp, J. (2011). The seeking mind: primal neuroaffective substrates for appetitive incentive states and their pathological dynamics in addictions and depression. Neurosci. Biobehav. Rev. 35, 1805-1820.
4. Alexander, G.E., Delong, M.R., and Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357-381.
5. Andero, R., Torras-Garcia, M., Quiroz-Padilla, M.F., Costa- Miserachs, D., and Coll-Andreu, M. (2007). Electrical stimulation of the pedunculopontine tegmental nucleus in freely moving awake rats: time- and site-specific effects on two-way active avoidance conditioning. Neurobiol. Learn. Mem. 87, 510-521.
6. Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A.M., and Kimura, M. (1994). Responses of tonically active neurons in the primates striatum undergo systematic changes during behavioral sensorimotor conditioning. J. Neurosci. 14, 3969-3984.
7. Ardayfio, P., Moon, J., Leung, K.K.A., Youn-Hwang, D., and Kim, K.-S. (2008). Impaired learning and memory in Pitx3 deficient aphakia mice: A genetic model for striatumdependent cognitive symptoms in Parkinson's disease. Neurobiol. Dis. 31, 406-412.
8. Bach, M.-E., Simpson, E.H., Kahn, L., Marshall, J.J., Kandel, E.R., and Kellendonk, C. (2008). Transient and selective overexpression of D-2 receptors in the striatum causes persistent deficits in conditional associative learning. Proc. Natl. Acad. Sci. USA 105, 16027-16032.
9. Baldo, B.A., Alsene, K.M., Negron, A., and Kelley, A.E. (2005). Hyperphagia induced by GABA(A) receptor-mediated inhibition of the nucleus accumbens shell: Dependence on intact neural output from the central amygdaloid region. Behav. Neurosci. 119, 1195-1206.
10. Balleine, B. (1992). Instrumental performance following a shift in primary motivation depends on incentive learning. J. Exp. Psychol. Anim. Behav. Process. 18, 236-250.
11. Balleine, B. and Dickinson, A. (1992). Signaling and incentive processes in instrumental reinforcer devaluation. Q. J. Exp. Psychol. B 45, 285-301.
12. Balleine, B.W. and O'Doherty, J.P. (2010). Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35, 48-69.
13. Balleine, B.W., Delgado, M.R., and Hikosaka, O. (2007). The role of the dorsal striatum in reward and decision-making. J. Neurosci. 27, 8161-8165.
14. Belin, D. and Everitt, B.J. (2008). Cocaine seeking habits depend upon doparnine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57, 432-441.
15. Belin, D., Jonkman, S., Dickinson, A., Robbins, T.W., and Everitt, B.J. (2009). Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav. Brain Res. 199, 89-102.
16. Berke, J.D., Breck, J.T., and Eichenbaum, H. (2009). Striatal versus hippocampal representations during win-stay maze performance. J. Neurophysiol. 101, 1575-1587.
17. Berridge, K.C. (2007). The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 131, 391-431.
18. Berridge, K.C. (2012). From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur. J. Neurosci. 35, 1124-1143.
19. Berridge, K.C., Robinson, T.E., and Aldridge, J.W. (2009). Dissecting components of reward:' liking ', ' wanting ', and learning. Curr. Opin. Pharmacol. 9, 65-73.
20. Bindra, D. (1978). How adaptive behavior is produced: a perceptualmotivational alternative to response-reinforcement. Behav. Brain Sci. 1, 41-97.
21. Blanchard, D.C. and Blanchard, R.J. (1988). Ethoexperimental approaches to the biology of emotion. Annu. Rev. Psychol. 39, 43-68.
22. Blundell, P., Hall, G., and Killcross, S. (2003). Preserved sensitivity to outcome value after lesions of the basolateral amygdala. J. Neurosci. 23, 7702-7709.
23. Bolles, R.C. (1970). Species-specific defense reactions and avoidance learning. Psychol. Rev. 77, 32-48.
24. Bolles, R.C. (1972). Reinforcement, expectancy, and learning. Psychol. Rev. 79, 394-409.
25. Bolles, R.C., Uhl, C.N., Wolfe, M., and Chase, P.B. (1975). Stimulus learning versus response learning in a discriminated punishment situation. Learn. Motiv. 6, 439-447.
26. Bortolanza, M., Wietzikoski, E.C., Boschen, S.L., Dombrowski, P., Latimer, M., MacLaren, D.A.A., Winn, P., and Da Cunha, C. (2010). Functional disconnection of the substantia nigra pars compacta from the pedunculopontine nucleus impairs learning of a conditioned avoidance task. Neurobiol. Learn. Mem. 94, 229-239.
27. Boschen, S.L., Wietzikoski, E.C., Winn, P., and Da Cunha, C. (2011). The role of nucleus accumbens and dorsolateral striatal D2 receptors in active avoidance conditioning. Neurobiol. Learn. Mem. 96, 254-262.
28. Bossert, J.M., Poles, G.C., Wihbey, K.A., Koya, E., and Shaham, Y. (2007). Differential effects of blockade of dopamine D-1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. J. Neurosci. 27, 12655-12663.
29. Bossert, J.M., Stern, A.L., Theberge, F.R.M., Marchant, N.J., Wang, H.-L., Morales, M., and Shaham, Y. (2012). Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking. J. Neurosci. 32, 4982-4991.
30. Bradfield, L.A. and McNally, G.P. (2010). The role of nucleus accumbens shell in learning about neutral versus excitatory stimuli during Pavlovian fear conditioning. Learn. Mem. 17, 337-343.
31. Broadbent, N.J., Squire, L.R., and Clark, R.E. (2007). Rats depend on habit memory for discrimination learning and retention. Learn. Mem. 14, 145-151.
32. Brown, J., Bullock, D., and Grossberg, S. (1999). How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues. J. Neurosci. 19, 10502-10511.
33. Buchanan, S.L. and Powell, D.A. (1982). Cingulate cortex - its role in Pavlovian conditioning. J. Comp. Physiol. Psychol. 96, 755-774.
34. Bunsey, M. and Eichenbaum, H. (1995). Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulus-stimulus association. Hippocampus 5, 546-556.
35. Burgess, N., Maguire, E.A., and O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron 35, 625-641.
36. Cabeza, R., Kapur, S., Craik, F.I.M., McIntosh, A.R., Houle, S., and Tulving, E. (1997). Functional neuroanatomy of recall and recognition: a PET study of episodic memory. J. Cogn. Neurosci. 9, 254-265.
37. Cassaday, H.J., Horsley, R.R., and Norman, C. (2005). Electrolytic lesions to nucleus accumbens core and shell have dissociable effects on conditioning to discrete and contextual cues in aversive and appetitive procedures respectively. Behav. Brain Res. 160, 222-235.
38. Chaudhri, N., Sahuque, L.L., and Janak, P.H. (2009). Ethanol seeking triggered by environmental context is attenuated by blocking dopamine D1 receptors in the nucleus accumbens core and shell in rats. Psychopharmacology 207, 303-314.
39. Chaudhri, N., Sahuque, L.L., Schairer, W.W., and Janak, P.H. (2010). Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking. Neuropsychopharmacology 35, 783-791.
40. Clark, R.E., West, A.N., Zola, S.M., and Squire, L.R. (2001). Rats with lesions of the hippocampus are impaired on the delayed nonmatching-to-sample task. Hippocampus 11, 176-186.
41. Cohen, N.J. and Squire, L.R. (1980). Preserved learning and retention of pattern-analyzing skill in amnesia - dissociation of knowing how and knowing that. Science 210, 207-210.
42. Cools, A.R. (1980). Role of the neostriatal dopaminergic activity in sequencing and selecting behavioral strategies - facilitation of processes involved in selecting the best strategy in a stressful situation. Behav. Brain Res. 1, 361-378.
43. Corbit, L.H., Muir, J.L., and Balleine, B.W. (2001). The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J. Neurosci. 21, 3251-3260.
44. D' Souza, M.S., Liechti, M.E., Ramirez-Nino, A.M., Kuczenski, R., and Markou, A. (2011). The metabotropic glutamate 2/3 receptor agonist LY379268 blocked nicotine-induced increases in nucleus accumbens shell dopamine only in the presence of a nicotine-associated context in rats. Neuropsychopharmacology 36, 2111-2124.
45. Da Cunha, C., Roozendaal, B., Vazdarjanova, A., and McGaugh, J.L. (1999). Microinfusions of flumazenil into the basolateral but not the central nucleus of the amygdala enhance memory consolidation in rats. Neurobiol. Learn. Mem. 72, 1-7.
46. Da Cunha, C., Gevaerd, M.S., Vital, M., Miyoshi, E., Andreatini, R., Silveira, R., Takahashi, R.N., and Canteras, N.S. (2001). Memory disruption in rats with nigral lesions induced by MPTP: a model for early Parkinson's disease amnesia. Behav. Brain Res. 124, 9-18.
47. Da Cunha, C., Silva, M.H.C., Wietzikoski, S., Wietzikoski, E.C., Ferro, M.M., Kouzmine, I., and Canteras, N.S. (2006). Place learning strategy of substantia nigra pars compacta-lesioned rats. Behav. Neurosci. 120, 1279-1284.
48. Da Cunha, C., Wietzikoski, S., Wietzikoski, E.C., Silva, M.H.C., Chandler, J., Ferro, M.M., Andreatini, R., and Canteras, N.S. (2007). Pre-training to find a hidden platform in the Morris water maze can compensate for a deficit to find a cued platform in a rat model of Parkinson's disease. Neurobiol. Learn. Mem. 87, 451-463.
49. Da Cunha, C., Wietzikoski, E.C., Dombrowski, P., Santos, L.M., Bortolanza, M., Boschen, S.L., and Miyoshi, E. (2009). Learning processing in the basal ganglia: a mosaic of broken mirrors. Behav. Brain Res. 199, 156-169.
50. Dalley, J.W. and Everitt, B.J. (2009). Dopamine receptors in the learning, memory and drug reward circuitry. Semin. Cell Dev. Biol. 20, 403-410.
51. Dayan, P. and Balleine, B.W. (2002). Reward, motivation, and reinforcement learning. Neuron 36, 285-98.
52. Delacour, J., Echavarria, M.T., and Senault, B. (1977). Specificity of learning deficits produced by micro-injections of 6-OHDA into nigro-striatal system of rat. Brain Res. 127, 384-385.
53. Descartes, R. (1989). The passions of the soul. In: An English Translation of Les Passions De L' Ame, S. H. Voss, ed. (Indianapolis, IN: Hacketting Publishing Company), pp. 1-165.
54. Devan, B.D., McDonald, R.J., and White, N.M. (1999). Effects of medial and lateral caudate-putamen lesions on placeand cue-guided behaviors in the water maze: relation to thigmotaxis. Behav. Brain Res. 100, 5-14.
55. Dezfouli, A. and Balleine, B.W. (2012). Habits, action sequences and reinforcement learning. Eur. J. Neurosci. 35, 1036-1051.
56. Di Chiara, G. (1995). The role of dopamine in drug abuse viewed from the perspective of its role in motivation. Drug Alcohol Depend. 8, 5-137.
57. Di Chiara, G. (2002). Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res. 137, 75-114.
58. Di Chiara, G., Bassareo, V., Fenu, S., De Luca, M.A., Spina, L., Cadoni, C., Acquas, E., Carboni, E., Valentini, V., and Lecca, D. (2004). Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47, 227-241.
59. Di Filippo, M., Picconi, B., Tantucci, M., Ghiglieri, V., Bagetta, V., Sgobio, C., Tozzi, A., Parnetti, L., and Calabresi, P. (2009). Short-term and long-term plasticity at corticostriatal synapses: implications for learning and memory. Behav. Brain Res. 199, 108-118.
60. Diamond, A. (1990). Rate of maturation of the hippocampus and the developmental progression of childrens performance on the delayed nonmatching to sample and visual paired comparison tasks. Ann. NY Acad. Sci. 608, 423-433.
61. Dickinson, A. and Balleine, B. (1994). Motivational control of goal-directed action. Anim. Learn. Behav. 22, 1-18.
62. Dickinson, A. and Balleine, B. (2002). The role of learning in the operation of motivational systems. Learning, motivation and emotion. In: Steven's Handbook of Experimental Psychology, C.R. Gallistel, ed. (New York: John Wiley and Sons), pp. 497-534.
63. Dombrowski, P.A., Maia, T.V., Boschen, S.L., Bortolanza, M., Wendler, E., Schwarting, R.K., Brandão, M.L., Winn, P., Blaha, C.D., and Da Cunha, C. (2012). Evidence that conditioned avoidance responses are reinforced by positive prediction errors signaled by tonic striatal dopamine. Behav. Brain Res. In press.
64. Dommett, E., Coizet, V., Blaha, C.D., Martindale, J., Lefebvre, V., Walton, N., Mayhew, J.E., Overton, P.G., and Redgrave, P. (2005). How visual stimuli activate dopaminergic neurons at short latency. Science 307, 1476-1479.
65. Edwards, S., Bachtell, R.K., Guzman, D., Whisler, K.N., and Self, D.W. (2011). Emergence of context-associated GluR(1) and ERK phosphorylation in the nucleus accumbens core during withdrawal from cocaine self-administration. Addict. Biol. 16, 450-457.
66. Eichenbaum, H. (2008). Learning and Memory (New York: Norton and Company).
67. Faure, A., Haberland, U., Conde, F., and El Massioui, N. (2005). Lesion to the nigrostriatal dopamine system disrupts stimulusresponse habit formation. J. Neurosci. 25, 2771-2780.
68. Faure, A., Reynolds, S.M., Richard, J.M., and Berridge, K.C. (2008). Mesolimbic dopamine in desire and dread: enabling motivation to be generated by localized glutamate disruptions in nucleus accumbens. J. Neurosci. 28, 7184-7192.
69. Faure, A., Leblanc-Veyrac, P., and El Massioui, N. (2010a). Dopamine agonists increase perseverative instrumental responses but do not restore habit formation in a rat model of parkinsonism. Neuroscience 168, 477-486.
70. Faure, A., Richard, J.M., and Berridge, K.C. (2010b). Desire and dread from the nucleus accumbens: cortical glutamate and subcortical GABA differentially generate motivation and hedonic impact in the rat. PLoS One 5, 13.
71. Fernandez-Ruiz, J., Wang, J., Aigner, T.G., and Mishkin, M. (2001). Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc. Natl. Acad. Sci. USA 98, 4196-4201.
72. Ferro, M.M., Bellissimo, M.I., Anselmo-Franci, J.A., Angellucci, M.E.M., Canteras, N.S., and Da Cunha, C. (2005). Comparison of bilaterally 6-OHDA- and MPTP-lesioned rats as models of the early phase of Parkinson's disease: Histological, neurochemical, motor and memory alterations. J. Neurosci. Methods 148, 78-87.
73. Flagel, S.B., Clark, J.J., Robinson, T.E., Mayo, L., Czuj, A., Willuhn, I., Akers, C.A., Clinton, S.M., Phillips, P.E.M., and Akil, H. (2011). A selective role for dopamine in stimulus-reward learning. Nature 469, 53-57.
74. Flaherty, A.W. and Graybiel, A.M. (1994). Input-output organization of the sensorimotor striatum in the squirrel-monkey. J. Neurosci. 14, 599-610.
75. Forster, G.L. and Blaha, C.D. (2003). Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat. Eur. J. Neurosci. 17, 751-762.
76. Frank, M.J. and Claus, E.D. (2006). Anatomy of a decision: striatoorbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychol. Rev. 113, 300-326.
77. Fredholm, B.B., Chen, J.F., Cunha, R.A., Svenningsson, P., and Vaugeois, J.M. (2005). Adenosine and brain function. Int. Rev. Neurobiol. 63, 191-270.
78. Gallagher, M. and Holland, P.C. (1994). The amygdala complex - multiple roles in associative learning and attention. Proc. Natl. Acad. Sci. USA 91, 11771-11776.
79. Gallagher, M., McMahan, R.W., and Schoenbaum, G. (1999). Orbitofrontal cortex and representation of incentive value in associative learning. J. Neurosci. 19, 6610-6614.
80. Gerardin, E., Lehericy, S., Pochon, J.B., Tezenas du Montcel, S., Mangin, J.F., Poupon, F., Agid, Y., Le Bihan, D., and Marsault, C. (2003). Foot, hand, face and eye representation in the human striatum. Cereb. Cortex 13, 162-169.
81. Gevaerd, M.S., Miyoshi, E., Silveira, R., Canteras, N.S., Takahashi, R.N., and Da Cunha, C. (2001a). L-dopa restores striatal dopamine level but fails to reverse MPTP-induced memory deficits in rats. Int. J. Neuropsycopharmacol. 4, 361-370.
82. Gevaerd, M.S., Takahashi, R.N., Silveira, R., and Da Cunha, C. (2001b). Caffeine reverses the memory disruption induced by intra-nigral MPTP-injection in rats. Brain Res. Bull. 55, 101-106.
83. Graziano, M. (2006). The organization of behavioral repertoire in motor cortex. Annu. Rev. Neurosci. 29, 105-134.
84. Graziano, M.S. and Gross, C.G. (1993). A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields. Exp. Brain Res. 97, 96-109.
85. Gurney, K., Prescott, T.J., and Redgrave, P. (2001). A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour. Biol. Cybern. 84, 411-423.
86. Guzowski, J.F., Setlow, B., Wagner, E.K., and McGaugh, J.L. (2001). Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 21, 5089-5098.
87. Haber, S.N. (2003). The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26, 317-330.
88. Haber, S.N. and Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4-26.
89. Hall, J., Parkinson, J.A., Connor, T.M., Dickinson, A., and Everitt, B.J. (2001). Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur. J. Neurosci. 13, 1984-1992.
90. Heimer, L., Zahm, D.S., Churchill, L., Kalivas, P.W., and Wohltmann, C. (1991). Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41, 89-125.
91. Hernandez-Lopez, S., Bargas, J., Surmeier, D.J., Reyes, A., and Galarraga, E. (1987). D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2 + conductance. J. Neurosci. Meth. 17, 3334-3342.
92. Hernandez-Lopez, S., Tkatch, T., Perez-Garci, E., Galarraga, E., Bargas, J., Hamm, H., and Surmeier, D.J. (2000). D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca currents and excitability via a novel PLC 1-IP-calcineurinsignaling cascade. J. Neurosci. 20, 8987-8995.
93. Hernandez, P.J., Sadeghian, K., and Kelley, A.E. (2002). Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens. Nat. Neurosci. 5, 1327-1331.
94. Hicks, L.H., Guilford, M.O., Moore, R.T., and Woodfork, C.A. (1979). Effects of lesions of the substantia nigra and subthalamic nucleus on place and response learning in the rat. Bull. Psychon. Soc. 14, 245-249.
95. Hikosaka, O., Sakamoto, M., and Usui, S. (1989). Functionalproperties of monkey caudate neurons. 2. Visual and auditory responses. J. Neurophysiol. 61, 799-813.
96. Ho, Y.J., Ho, S.C., Pawlak, C.R., and Yeh, K.Y. (2011). Effects of D-cycloserine on MPTP-induced behavioral and neurological changes: potential for treatment of Parkinson's disease dementia. Behav. Brain Res. 219, 280-290.
97. Holland, P.C. and Bouton, M.E. (1999). Hippocampus and context in classical conditioning. Curr. Opin. Neurobiol. 9, 195-202.
98. Hull, C.L. (1930). Knowledge and purpose as habit mechanism. Psychol. Rev. 30, 511-525.
99. Hull, C.L. (1931). Goal attraction and directing ideas conceived as habit phenomena. Psychol. Rev. 38, 487-506.
100. Hull, C.L. (1943). Principles of Behavior (New York: Appleton-Century- Crofts).
101. Humphries, M.D. and Prescott, T.J. (2010). The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog. Neurobiol. 90, 385-417.
102. Ikemoto, S. (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbensolfactory tubercle complex. Brain Res. Rev. 56, 27-78.
103. Ikemoto, S. and Panksepp, J. (1999). The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res. Rev. 31, 6-41.
104. Isoda, M. and Hikosaka, O. (2011). Cortico-basal ganglia mechanisms for overcoming innate, habitual and motivational behaviors. Eur. J. Neurosci. 33, 2058-2069.
105. Ito, R., Robbins, T.W., and Everitt, B.J. (2004). Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat. Neurosci. 7, 389-397.
106. Ito, R., Robbins, T.W., Pennartz, C.M., and Everitt, B.J. (2008). Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning. J. Neurosci. 28, 6950-6959.
107. Izquierdo, I., Da Cunha, C., Rosat, R., Jerusalinsky, D., Ferreira, M.B.C., and Medina, J.H. (1992). Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behav. Neural. Biol. 58, 16-26.
108. Izquierdo, A., Suda, R.K., and Murray, E.A. (2004). Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J. Neurosci. 24, 7540-7548.
109. Izquierdo, I., Bevilaqua, L.R.M., Rossato, J.I., Bonini, J.S., Medina, J.H., and Cammarota, M. (2006). Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 29, 496-505.
110. Jahanshahi, M., Ardouin, C.M.A., Brown, R.G., Rothwell, J.C., Obeso, J., Albanese, A., Rodriguez-Oroz, M.C., Moro, E., Benabid, A.L., Pollak, P., et al. (2000). The impact of deep brain stimulation on executive function in Parkinson's disease. Brain 123, 1142-1154.
111. Jenkins, I.H., Brooks, D.J., Nixon, P.D., Frackowiak, R.S.J., and Passingham, R.E. (1994). Motor sequence learning - a study with positron emission tomography. J. Neurosci. 14, 3775-3790.
112. Jog, M.S., Kubota, Y., Connolly, C.I., Hillegaart, V., and Graybiel, A.M. (1999). Building neural representations of habits. Science 286, 1745-1749.
113. Jonkman, S. and Everitt, B.J. (2011). Dorsal and ventral striatal protein synthesis inhibition affect reinforcer valuation but not the consolidation of instrumental learning. Learn. Mem. 18, 617-624.
114. Kawaguchi, Y., Wilson, C.J., Augood, S.J., and Emson, P.C. (1995). Striatal interneurons - chemical, physiological and morphological characterization. Trends Neurosci. 18, 527-535.
115. Kelsey, J.E., Gerety, L.P., and Guerriero, R.M. (2009). Electrolytic lesions of the nucleus accumbens core (but not the medial shell) and the basolateral amygdala enhance context-specific locomotor sensitization to nicotine in rats. Behav. Neurosci. 123, 577-588.
116. Knowlton, B.J., Mangels, J.A., and Squire, L.R. (1996). A neostriatal habit learning system in humans. Science 273, 1399-1402.
117. Krause, M., German, P.W., Taha, S.A., and Fields, H.L. (2010). A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. J. Neurosci. 30, 4746-4756.
118. Kreitzer, A.C. and Berke, J.D. (2011). Investigating striatal function through cell-type-specific manipulations. Neuroscience 198, 19-26.
119. Kropotov, J.D. and Etlinger, S.C. (1999). Selection of actions in the basal ganglia thalamocortical circuits: review and model. Int. J. Psychophysiol. 31, 197-217.
120. Latham, G.P. and Pinder, C.C. (2005). Work motivation theory and research at the dawn of the twenty-first century. Annu. Rev. Psychol. 56, 485-516.
121. Leea, A.S., Duman, R.S., and Pittenger, C. (2008). A double dissociation revealing bidirectional competition between striatum and hippocampus during learning. Proc. Natl. Acad Sci. USA 105, 17163-17168.
122. Lester, D.B., Rogers, T.D., and Blaha, C.D. (2010). Acetylcholinedopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci. Ther. 16, 137-162.
123. Levita, L., Dalley, J.W., and Robbins, T.W. (2000). Excitotoxic lesions of the nucleus accumbens core impair contextual but not discrete cue pavlovian aversive conditioning. Eur. J. Neurosci. 12, 88-98.
124. Lewis, B.L. and O'Donnell, P. (2000). Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential' up ' states in pyramidal neurons via D-1 dopamine receptors. Cereb. Cortex. 10, 1168-1175.
125. Lingawi, N.W. and Balleine, B.W. (2012). Amygdala central nucleus interacts with dorsolateral striatum to regulate the acquisition of habits. J. Neurosci. 32, 1073-1081.
126. Lobo, M.K., Cui, Y., Ostlund, S.B., Balleine, B.W., and Yang, X.W. (2007). Genetic control of instrumental conditioning by striatopallidal neuron - specific S1P receptor Gpr6. Nat. Neurosci. 10, 1395-1397.
127. Lovibond, P.F. (1983). Facilitation of instrumental behavior by a Pavlovian appetitive conditioned-stimulus. J. Exp. Psychol. Anim. Behav. Process. 9, 225-247.
128. Lovinger, D.M. (2010). Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58, 951-961.
129. Machado, A., Haber, S., Sears, N., Greenberg, B., Malone, D., and Rezai, A. (2009). Functional topography of the ventral striatum and anterior limb of the internal capsule determined by electrical stimulation of awake patients. Clin. Neurophysiol. 120, 1941-1948.
130. Mackintosh, N.J. (1974). The Psychology of Animal Learning. (London: Academic Press).
131. Maguire, E.A., Gadian, D.G., Johnsrude, I.S., Good, C.D., Ashburner, J., Frackowiak, R.S.J., and Frith, C.D. (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. USA 97, 4398-4403.
132. Maldonado, I.C.S., Swanson, C.J., and Kelley, A.E. (1995). Glutamate receptors in the nucleus-accumbens shell control feedingbehavior via the lateral hypothalamus. J. Neurosci. 15, 6779-6788.
133. Maren, S., Aharonov, G., and Fanselow, M.S. (1997). Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res. 88, 261-274.
134. Matsumoto, N., Hanakawa, T., Maki, S., Graybiel, A.M., and Kimura, M. (1999). Role of [corrected] nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J. Neurophysiol. 82, 978-998.
135. May, P.J., McHaffie, J.G., Stanford, T.R., Jiang, H., Costello, M.G., Coizet, V., Hayes, L.M., Haber, S.N., and Redgrave, P. (2009). Tectonigral projections in the primate: a pathway for pre-attentive sensory input to midbrain dopaminergic neurons. Eur. J. Neurosci. 29, 575-587.
136. McDonald, R.J. and White, N.M. (1993). A triple dissociation of memory-systems - hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 107, 3-22.
137. McDonald, R.J. and White, N.M. (1994). Parallel informationprocessing in the water maze - evidence for independent memory-systems involving dorsal striatum and hippocampus. Behav. Neural Biol. 61, 260-270.
138. McDonald, R.J., Devan, B.D., and Hong, N.S. (2004). Multiple memory systems: the power of interactions. Neurobiol. Learn. Mem. 82, 333-346.
139. McHaffie, J.G., Stanford, T.R., Stein, B.E., Coizet, W., and Redgrave, P. (2005). Subcortical loops through the basal ganglia. Trends Neurosci. 28, 401-407.
140. Meredith, G.E., Baldo, B.A., Andrezjewski, M.E., and Kelley, A.E. (2008). The structural basis for mapping behavior onto the ventral striatum and its subdivisions. Brain Struct. Funct. 213, 17-27.
141. Meunier, M., Bachevalier, J., Mishkin, M., and Murray, E.A. (1993). Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesusmonkeys. J. Neurosci. 13, 5418-5432.
142. Miller, N.E. (1951). Learnable drives and reward. In: Handbook of Experimental Psychology, S.S. Stevens, ed. (New York: Wiley), pp. 435-472.
143. Mink, J.W. (1996). The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381-425.
144. Mitcham, J.C. and Thomas, R.K. (1972). Effects of substantia nigra and caudate-nucleus lesions on avoidance-learning in rats. J. Comp. Physiol. Psychol. 81, 101-107.
145. Miyoshi, E., Wietzikoski, S., Camplessei, M., Silveira, R., Takahashi, R.N., and Da Cunha, C. (2002). Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions. Brain Res. Bull. 58, 41-47.
146. Miyoshi, E., Wietzikoski, E.C., Bortolanza, M., Boschen, S.L., Canteras, N.S., Izquierdo, I., and Da Cunha, C. (2012). Both the dorsal hippocampus and the dorsolateral striatum are needed for rat navigation in the Morris water maze. Behav. Brain Res. 226, 171-178.
147. Mizumori, S.J.Y., Yeshenko, O., Gill, K.M., and Davis, D.M. (2004). Parallel processing across neural systems: implications for a multiple memory system hypothesis. Neurobiol. Learn. Mem. 82, 278-298.
148. Mogenson, G.J., Jones, D.L., and Yim, C.Y. (1980). From motivation to action - functional interface between the limbic system and the motor system. Prog. Neurobiol. 14, 69-97.
149. Moreira, C.G., Barbiero, J.K., Ariza, D., Dombrowski, P.A., Sabioni, P., Bortolanza, M., Da Cunha, C., Vital, M., and Lima, M.M.S. (2012). Behavioral, neurochemical and histological alterations promoted by bilateral intranigral rotenone administration: A new approach for an old neurotoxin. Neurotox. Res. 2 1, 291-3 01.
150. Morris, R.G.M., Garrud, P., Rawlins, J.N.P., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
151. Nagy, A., Eordegh, G., Paroczy, Z., Markus, Z., and Benedek, G. (2006). Multisensory integration in the basal ganglia. Eur. J. Neurosci. 24, 917-924.
152. Nambu, A., Kaneda, K., Tokuno, H., and Takada, M. (2002a). Organization of corticostriatal motor inputs in monkey putamen. J. Neurophysiol. 88, 1830-1842.
153. Nambu, A., Tokuno, H., and Takada, M. (2002b). Functional significance of the cortico-subthalamo-pallidal ' hyperdirect' pathway. Neurosc. Res. 43, 111-117.
154. Nestler, E.J. and Carlezon, W.A. (2006). The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59, 1151-1159.
155. Nicola, S.M. (2007). The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology 191, 521-550.
156. Nikolaus, S., Huston, J.P., Korber, B., Thiel, C., and Schwarting, R.K.W. (1997). Pretreatment with neurokinin substance P but not with cholecystokinin-8S can alleviate functional deficits of partial nigrostriatal 6-hydroxydopamine lesion. Peptides 18, 1161-1168.
157. Obeso, J.A., Rodriguez-Oroz, M.C., Benitez-Temino, B., Blesa, F.J., Guridi, J., Marin, C., and Rodriguez, M. (2008). Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Mov. Disord. 23, S548 - S559.
158. Olton, D.S., Becker, J.T., and Handelmann, G.E. (1979). Hippocampus, apace, and memory. Behav. Brain Sci. 2, 313-322.
159. Packard, M.G. and Knowlton, B.J. (2002). Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 25, 563-593.
160. Packard, M.G. and McGaugh, J.L. (1992). Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav. Neurosci. 106, 439-446.
161. Packard, M.G. and McGaugh, J.L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 65, 65-72.
162. Packard, M.G. and White, N.M. (1990). Lesions of the caudatenucleus selectively impair reference memory acquisition in the radial maze. Behav. Neural Biol. 53, 39-50.
163. Packard, M.G. and White, N.M. (1991). Dissociation of hippocampus and caudate-nucleus memory-systems by posttraining intracerebral injection of dopamine agonists. Behav. Neurosci. 105, 295-306.
164. Packard, M.G., Hirsh, R., and White, N.M. (1989). Differentialeffects of fornix and caudate-nucleus lesions on 2 radial maze tasks - evidence for multiple memory-systems. J. Neurosci. 9, 1465-1472.
165. Packard, M.G., Winocur, G., and White, N.M. (1992). The caudate-nucleus and acquisition of win shift radial-maze behavior - effect of exposure to the reinforcer during maze adaptation. Psychobiology 20, 127-132.
166. Panksepp, J. (1982). Toward a general psycho-biological theory of emotions. Behav. Brain Sci. 5, 407-422.
167. Parent, A. and Hazrati, L.N. (1995a). Functional-anatomy of the basal ganglia. 1. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Rev. 20, 91-127.
168. Parent, A. and Hazrati, L.N. (1995b). Functional-anatomy of the basal ganglia. 2. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Rev. 20, 128-154.
169. Parkinson, J.A., Robbins, T.W., and Everitt, B.J. (1999). Selective excitotoxic lesions of the nucleus accumbens core and shell differentially affect aversive Pavlovian conditioning to discrete and contextual cues. Psychobiology 27, 256-266.
170. Parkinson, J.A., Willoughby, P.J., Robbins, T.W., and Everitt, B.J. (2000). Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behav. Neurosci. 114, 42-63.
171. Pavlov, P.I. (1927). Conditioned Reflexes (London: Oxford University Press).
172. Perry, J.C., Da Cunha, C., Anselmo-Franci, J., Andreatini, R., Miyoshi, E., Tufik, S., and Vital, M. (2004). Behavioural and neurochemical effects of phosphatidylserine in MPTP lesion of the substantia nigra of rats. Eur. J. Pharmacol. 484, 225-233.
173. Pezze, M.A., Heidbreder, C.A., Feldon, J., and Murphy, C.A. (2001). Selective responding of nucleus accumbens core and shell dopamine to aversively conditioned contextual and discrete stimuli. Neuroscience 108, 91-102.
174. Phillips, R.G. and Ledoux, J.E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285.
175. Pijnenbu, A.J. and Vanrossu, J.M. (1973). Stimulation of locomotor activity following injection of dopamine into nucleus accumbens. J. Pharm. Pharmacol. 25, 1003-1005.
176. Prensa, L., Gimenez-Amaya, J.M., Parent, A., Bernácer, J., and Cebrián, C. (2009). The nigrostriatal pathway: axonal collateralization and compartmental specificity. In: Birth, Life and Death of Dopaminergic Neurons in the Substantia Nigra, G. Di Giovanni, V. Di Matteo, G. Esposito, eds. (Wein, NY: Springer-Verlag), pp. 49-58.
177. Redgrave, P., Rodriguez, M., Smith, Y., Rodriguez-Oroz, M.C., Lehericy, S., Bergman, H., Agid, Y., DeLong, M.R., and Obeso, J.A. (2010). Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat. Rev. Neurosci. 11, 760-772.
178. Redgrave, P., Vautrelle, N., and Reynolds, J.N.J. (2011). Functional properties of the basal ganglia's re-entrant loop architecture: selection and reinforcement. Neuroscience 198, 138-151.
179. Reeve, A. (2009). Understanding Motivation and Emotion (New York: John Wiley and Sons).
180. Rescorla, R.A. and Solomon, R.L. (1967). Two-process learning theory - relationships between Pavlovian conditioning and instrumental learning. Psychol. Rev. 74, 151-182.
181. Reynolds, S.M. and Berridge, K.C. (2001). Fear and feeding in the nucleus accumbens shell: rostrocaudal segregation of GABA-elicited defensive behavior versus eating behavior. J. Neurosci. 21, 3261-3270.
182. Reynolds, S.M. and Berridge, K.C. (2002). Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste " liking"/" disliking" reactions, place preference/avoidance, and fear. J. Neurosci. 22, 7308-7320.
183. Reynolds, S.M. and Berridge, K.C. (2008). Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat. Neurosci. 11, 423-425.
184. Riedel, G., Harrington, N.R., Hall, G., and Macphail, E.M. (1997). Nucleus accumbens lesions impair context, but not cue, conditioning in rats. Neuroreport 8, 2477-2481.
185. Rizley, R.C. and Rescorla, R.A. (1972). Associations in second-order conditioning and sensory preconditioning. J. Comp. Physiol. Psychol. 81, 1-8.
186. Robbins, T.W. (1976). Relationship between reward-enhancing and stereotypical effects of psychomotor stimulant-drugs. Nature 264, 57-59.
187. Roitman, M.F., Wheeler, R.A., Tiesinga, P.H.E., Roitman, J.D., and Carelli, R.M. (2010). Hedonic and nucleus accumbens neural responses to a natural reward are regulated by aversive conditioning. Learn. Mem. 17, 539-546.
188. Routtenberg, A. and Holzman, N. (1973). Memory disruption by electrical-stimulation of substantia nigra, pars compacta. Science 181, 83-86.
189. Satorra-Marin, N., Homs-Ormo, S., Arevalo-Garcia, R., Morgado- Bernal, I., and Coll-Andreu, M. (2006). Effects of pre-training pedunculopontine tegmental nucleus lesions on delayed matching- and non-matching-to-position in a T-maze in rats. Behav. Brain Res. 160, 115-124.
190. Schmidt, L.S., Miller, A.D., Lester, D.B., Bay-Richter, C., Schulein, C., Frikke-Schmidt, H., Wess, J., Blaha, C.D., Woldbye, D.P.D., Fink-Jensen, A., et al. (2010). Increased amphetamine-induced locomotor activity, sensitization, and accumbal dopamine release in M(5) muscarinic receptor knockout mice. Psychopharmacology 207, 547-558.
191. Schroeder, J.P., Wingard, J.C., and Packard, M.G. (2002). Post-training reversible inactivation of hippocampus reveals interference between memory systems. Hippocampus 12, 280-284.
192. Schultz, W. (2007). Behavioral dopamine signals. Trends Neurosci. 30, 203-10.
193. Schumacher, A., de Vasconcelos, A.P., Lecourtier, L., Moser, A., and Cassel, J.-C. (2011). Electrical high frequency stimulation in the dorsal striatum: effects on response learning and on GABA levels in rats. Behav. Brain Res. 222, 368-374.
194. Scoville, W.B. and Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11-21.
195. Sesack, S.R. and Grace, A.A. (2010). Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35, 27-47.
196. Shin, R., Cao, J.R., Webb, S.M., and Ikemoto, S. (2010). Amphetamine administration into the ventral striatum facilitates behavioral interaction with unconditioned visual signals in rats. PLoS One 5, e8741.
197. Skinner, B.F. (1938). The Behavior of Organisms (New York: Appleton-Century-Crofts).
198. Smith-Roe, S.L. and Kelley, A.E. (2000). Coincident activation of NMDA and dopamine D-1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J. Neurosci. 20, 7737-7742.
199. Smith, K.S., Berridge, K.C., and Aldridge, J.W. (2011). Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc. Natl. Acad. Sci. USA 108, E255 - E264.
200. Son, J.H., Latimer, C. and Keefe, K.A. (2011). Impaired formation of stimulus-response, but not action-outcome, associations in rats with methamphetamine-induced neurotoxicity. Neuropsychopharmacology 36, 2441-2451.
201. Spence, K.W. (1956). Behavior Theory and Conditioning (New Haven: Yale Press).
202. Squire, L.R. and Zola, S.M. (1996). Structure and function of declarative and nondeclarative memory systems. Proc. Natl. Acad. Sci. USA 93, 13515-13522.
203. Staddon, J.E.R. (2003). Adaptative Behavior and Learning (New York: Cambridge University Press).
204. Staubli, U. and Huston, J.P. (1978). Task-dependent effects of post-trial reinforcing or sub-reinforcing stimulation of substantia nigra on avoidance-learning. Experientia 34, 903-903.
205. Steckler, T., Inglis, W., Winn, P., and Sahgal, A. (1994). The pedunculopontine tegmental nucleus - a role in cognitive-processes. Brain Res. Rev. 19, 298-318.
206. Stern, E.A., Kincaid, A.E., and Wilson, C.J. (1997). Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77, 1697-1715.
207. Stratford, T.R. and Kelley, A.E. (1999). Evidence of a functional relationship between the nucleus accumbens shell and lateral hypothalamus subserving the control of feeding behavior. J. Neurosci. 19, 11040-11048.
208. Stratford, T.R., Swanson, C.J., and Kelley, A. (1998). Specific changes in food intake elicited by blockade or activation of glutamate receptors in the nucleus accumbens shell. Behav. Brain Res. 93, 43-50.
209. Swanson, L.W. and Cowan, W.M. (1975). Connections and development of nucleus accumbens. Brain Res. 92, 324-330.
210. Tadaiesky, M.T., Dombrowski, P.A., Figueiredo, C.P., Cargnin- Ferreira, E., Da Cunha, C., and Takahashi, R.N. (2008). Emotional, cognitive and neurochemical alterations in a premotor stage model of Parkinson's disease. Neuroscience 156, 830-840.
211. Takakusaki, K., Saitoh, K., Harada, H., and Kashiwayanagi, M. (2004). Role of basal ganglia-brainstem pathways in the control of motor behaviors. Neurosc. Res. 50, 137-151.
212. Tang, C.K., Pawlak, A.P., Prokopenko, V., and West, M.O. (2007). Changes in activity of the striatum during formation of a motor habit. Eur. J. Neurosci. 25, 1212-1227.
213. Thompson, R.F. and Steinmetz, J.E. (2009). The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162, 732-755.
214. Thorndike, E.L. (1911). Animal Intelligence (New York: Macmillan).
215. Tolman, E.C. (1959). Conductismo molar e intencional. In: Psychological Theory, M. Marx, ed. (New York: Macmillan), pp. 410-428.
216. Trapold, M.A., Lawton, G.W., Dick, R.A., and Gross, D.M. (1968). Transfer of training from differential classical to differential instrumental conditioning. J. Exp. Psychol. 76, 568-584.
217. Vale-Martinez, A., Baxter, M.G., and Eichenbaum, H. (2002). Selective lesions of basal forebrain cholinergic neurons produce anterograde and retrograde deficits in a social transmission of food preference task in rats. Eur. J. Neurosci. 16, 983-998.
218. van Wouwe, N.C., Ridderinkhof, K.R., van den Wildenberg, W.P.M., Band, G.P.H., Abisogun, A., Elias, W.J., Frysinger, R., and Wylie, S.A. (2011). Deep brain stimulation of the subthalamic nucleus improves reward-based decision-learning in Parkinson's disease. Front. Hum. Neurosci. 5, 1-13.
219. Vazdarjanova, A. and McGaugh, J.L. (1999). Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J. Neurosci. 19, 6615-6622.
220. Vianna, M.R., Coitinho, A.S., and Izquierdo, I. (2004). Role of the hippocampus and amygdala in the extinction of fear-motivated learning. Curr. Neurovasc. Res. 1, 55-60.
221. Voorn, P., Vanderschuren, L., Groenewegen, H.J., Robbins, T.W., and Pennartz, C.M.A. (2004). Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27, 468-474.
222. West, A.R. and Grace, A.A. (2000). Striatal nitric oxide signaling regulates the neuronal activity of midbrain dopamine neurons in vivo. J. Neurophysiol. 83, 1796-1808.
223. White, N.M. (2009). Some highlights of research on the effects of caudate nucleus lesions over the past 200 years. Behav. Brain Res. 199, 3-23.
224. White, N.M. and McDonald, R.J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 77, 125-184.
225. Wietzikoski, E.C., Boschen, S.L., Miyoshi, E., Bortolanza, M., Santos, L.M., Frank, M., Brandão, M.L., Winn, P., and Da Cunha, C. (2012). Roles of D1-like dopamine receptors in the nucleus accumbens and dorsolateral striatum in conditioned avoidance response. Psychopharmacology 219, 159-169.
226. Wilson, D.I.G., MacLaren, D.A.A., and Winn, P. (2009). Bar pressing for food: differential consequences of lesions to the anterior versus posterior pedunculopontine. Eur. J. Neurosci. 30, 504-513.
227. Wise, R.A. (2008). Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox. Res. 14, 169-183.
228. Woodwoth, R.S. (1918). Dynamic Psychology (New York: Columbia University Press).
229. Yin, H.H. and Knowlton, B.J. (2006). The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464-476.
230. Yin, H.H., Knowlton, B.J., and Balleine, B.W. (2004). Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 19, 181-189.
231. Yin, H.H., Knowlton, B.J., and Balleine, B.W. (2005a). Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur. J. Neurosci. 22, 505-512.
232. Yin, H.H., Ostlund, S.B., Knowlton, B.J., and Balleine, B.W. (2005b). The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 22, 513-523.
233. Yin, H.H., Knowlton, B.J., and Balleine, B.W. (2006). Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav. Brain Res. 166, 189-196.
234. Yin, H.H., Ostlund, S.B., and Balleine, B.W. (2008). Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur. J. Neurosci. 28, 1437-1448.
235. Yu, C., Gupta, J., Chen, J.-F., and Yin, H.H. (2009). Genetic deletion of A(2A) adenosine receptors in the striatum selectively impairs habit formation. J. Neurosci. 29, 15100-15103.