The role of the basal ganglia in learning and memory: Insight from Parkinson's disease

Neurobiology of Learning and Memory

Volumn 96, Issue 4, 2011, Pages 624-636

  Foerde, Karin ^a   Shohamy, Daphna ^a  

^a Howard Hughes Medical Institute   (United States)

Author keywords

Dopamine; Hippocampus; Learning; Parkinson's disease; Striatum

Indexed keywords

DOPAMINE;

BASAL GANGLION; BRAIN CORTEX; BRAIN REGION; DECISION MAKING; DECLARATIVE MEMORY; FEEDBACK SYSTEM; HUMAN; LEARNING; MEMORY; MOTIVATION; NEUROSCIENCE; PARKINSON DISEASE; PUNISHMENT; REVIEW; REWARD; STIMULUS RESPONSE; TEMPORAL LOBE;

BASAL GANGLIA; HUMANS; LEARNING; MEMORY; PARKINSON DISEASE;

EID: 82355181048     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.08.006     Document Type: Review

References (169)

1. Adams C.D., Dickinson A. Instrumental responding following reinforcer devaluation. Quarterly Journal of Experimental Psychology 1981, 33:109-122.
2. Adcock R.A., Thangavel A., Whitfield-Gabrieli S., Knutson B., Gabrieli J.D. Reward-motivated learning: Mesolimbic activation precedes memory formation. Neuron 2006, 50(3):507-517.
3. Biochemistry of neurotransmitters in Parkinson's disease. (Vol. 2) 1987, Butterworth's and Co, London. Y. Agid, M. Javoy-Agid, M. Ruberg (Eds.).
4. Aizenstein H.J., Stenger V.A., Cochran J., Clark K., Johnson M., Nebes R.D., et al. Regional brain activation during concurrent implicit and explicit sequence learning. Cerebral Cortex 2004, 14(2):199-208.
5. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 1986, 9:357-381.
6. Aron A.R., Shohamy D., Clark J., Myers C., Gluck M.A., Poldrack R.A. Human midbrain sensitivity to cognitive feedback and uncertainty during classification learning. Journal of Neurophysiology 2004, 92(2):1144-1152.
7. Ashby F.G., Noble S., Filoteo J.V., Waldron E.M., Ell S.W. Category learning deficits in Parkinson's disease. Neuropsychology 2003, 17(1):115-124.
8. Bäckman L., Ginovart N., Dixon R.A., Wahlin T.B., Wahlin A., Halldin C., et al. Age-related cognitive deficits mediated by changes in the striatal dopamine system. American Journal of Psychiatry 2000, 157(4):635-637.
9. Bakker A., Kirwan C.B., Miller M., Stark C.E. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319(5870):1640-1642.
10. Balleine B.W., O'Doherty J.P. Human and rodent homologies in action control: Corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 2010, 35(1):48-69.
11. Barnes T.D., Mao J.B., Hu D., Kubota Y., Dreyer A.A., Stamoulis C., et al. Advance-cueing produces enhanced action-boundary patterns of spike activity in the sensorimotor striatum. Journal of Neurophysiology 2011.
12. Bernheimer H., Birkmayer W., Hornykiewicz O., Jellinger K., Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. Journal of the Neurological Sciences 1973, 20(4):415-455.
13. Brainard M.S., Doupe A.J. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 2000, 404(6779):762-766.
14. Breitenstein C., Korsukewitz C., Floel A., Kretzschmar T., Diederich K., Knecht S. Tonic dopaminergic stimulation impairs associative learning in healthy subjects. Neuropsychopharmacology 2006, 31(11):2552-2564.
15. Brischoux F., Chakraborty S., Brierley D.I., Ungless M.A. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(12):4894-4899.
16. Cavaco S., Anderson S.W., Allen J.S., Castro-Caldas A., Damasio H. The scope of preserved procedural memory in amnesia. Brain 2004, 127(Pt 8):1853-1867.
17. Chang Q., Gold P.E. Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behavioral Brain Research 2003, 144(1-2):19-24.
18. Chang Q., Gold P.E. Switching memory systems during learning: Changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. Journal of Neuroscience 2003, 23(7):3001-3005.
19. Chun M.M., Phelps E.A. Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nature Neuroscience 1999, 2(9):844-847.
20. Cincotta C.M., Seger C.A. Dissociation between striatal regions while learning to categorize via feedback and via observation. Journal of Cognitive Neuroscience 2007, 19(2):249-265.
21. Cohen M.X., Schoene-Bake J.C., Elger C.E., Weber B. Connectivity-based segregation of the human striatum predicts personality characteristics. Nature Neuroscience 2009, 12(1):32-34.
22. Cohen N.J., Eichenbaum H. Memory 1993, The MIT Press amnesia, and the hippocampal system, Cambridge, MA, US.
23. Cohn M., Moscovitch M., Davidson P.S. Double dissociation between familiarity and recollection in Parkinson's disease as a function of encoding tasks. Neuropsychologia 2010, 48(14):4142-4147.
24. Cools R., Altamirano L., D'Esposito M. Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 2006, 44(10):1663-1673.
25. Cools R., Barker R.A., Sahakian B.J., Robbins T.W. Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. Cerebral Cortex 2001, 11(12):1136-1143.
26. Cools R., Frank M.J., Gibbs S.E., Miyakawa A., Jagust W., D'Esposito M. Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. Journal of Neuroscience 2009, 29(5):1538-1543.
27. Cools R., Lewis S.J., Clark L., Barker R.A., Robbins T.W. L-dopa disrupts activity in the nucleus accumbens during reversal learning in Parkinson's disease. Neuropsychopharmacology 2007, 32(1):180-189.
28. Curran T., Keele S.W. Attentional and nonattentional forms of sequence learning. Journal of Experimental Psychology: Learning, Memory, & Cognition. 1993, 19(1):189-202.
29. D'Ardenne K., McClure S.M., Nystrom L.E., Cohen J.D. BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 2008, 319(5867):1264-1267.
30. Daselaar S.M., Fleck M.S., Cabeza R. Triple dissociation in the medial temporal lobes: Recollection, familiarity, and novelty. Journal of Neurophysiology 2006, 96(4):1902-1911.
31. Davachi L. Item, context and relational episodic encoding in humans. Current Opinion in Neurobiology 2006, 16(6):693-700.
32. Davidson P.S., Anaki D., Saint-Cyr J.A., Chow T.W., Moscovitch M. Exploring the recognition memory deficit in Parkinson's disease: Estimates of recollection versus familiarity. Brain 2006, 129(Pt 7):1768-1779.
33. Delgado M.R. Reward-related responses in the human striatum. Annals of the New York Academy of Sciences 2007, 1104:70-88.
34. Delgado M.R., Locke H.M., Stenger V.A., Fiez J.A. Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations. Cognitive Affect Behavioral Neuroscience 2003, 3(1):27-38.
35. 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. Journal of Neurophysiology 2000, 84(6):3072-3077.
36. Deutch A.Y., Cameron D.S. Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell. Neuroscience 1992, 46(1):49-56.
37. Di Martino A., Scheres A., Margulies D.S., Kelly A.M., Uddin L.Q., Shehzad Z., et al. Functional connectivity of human striatum: A resting state FMRI study. Cerebral Cortex 2008, 18(12):2735-2747.
38. Dickerson K.C., Li J., Delgado M.R. Parallel contributions of distinct human memory systems during probabilistic learning. Neuroimage 2010.
39. Diedrichsen J., Hashambhoy Y., Rane T., Shadmehr R. Neural correlates of reach errors. Journal of Neuroscience 2005, 25(43):9919-9931.
40. Divac I., Rosvold H.E., Szwarcbart M.K. Behavioral effects of selective ablation of the caudate nucleus. Journal of Comparative and Physiological Psychology 1967, 63(2):184-190.
41. Doeller C.F., King J.A., Burgess N. Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(15):5915-5920.
42. Doyon J. Motor sequence learning and movement disorders. Current Opinion in Neurology 2008, 21(4):478-483.
43. Doyon J., Penhune V., Ungerleider L.G. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 2003, 41(3):252-262.
44. Doyon J., Gaudreau D., Laforce R., Castonguay M., Bedard P.J., Bedard F., et al. Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain and Cognition 1997, 34(2):218-245.
45. Doyon J., Laforce R., Bouchard G., Gaudreau D., Roy J., Poirier M., et al. Role of the striatum, cerebellum and frontal lobes in the automatization of a repeated visuomotor sequence of movements. Neuropsychologia 1998, 36(7):625-641.
46. Duzel E., Bunzeck N., Guitart-Masip M., Duzel S. NOvelty-related motivation of anticipation and exploration by dopamine (NOMAD): Implications for healthy aging. Neuroscience and Biobehavioral Reviews 2010, 34(5):660-669.
47. Duzel E., Bunzeck N., Guitart-Masip M., Wittmann B., Schott B.H., Tobler P.N. Functional imaging of the human dopaminergic midbrain. Trends in Neurosciences 2009, 32(6):321-328.
48. Eichenbaum H., Fagan A., Mathews P., Cohen N.J. Hippocampal system dysfunction and odor discrimination learning in rats: Impairment or facilitation depending on representational demands. Behavioral Neuroscience 1988, 102(3):331-339.
49. Fiorillo C.D., Newsome W.T., Schultz W. The temporal precision of reward prediction in dopamine neurons. Nature Neuroscience 2008, 11(8):966-973.
50. Fiorillo C.D., Tobler P.N., Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 2003, 299(5614):1898-1902.
51. Foerde K., Knowlton B.J., Poldrack R.A. Modulation of competing memory systems by distraction. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(31):11778-11783.
52. Foerde K., Shohamy D. Feedback timing modulates brain systems for learning in humans. Journal of Neuroscience 2011, 31(37):13157-13167.
53. Frank M.J. Dynamic dopamine modulation in the basal ganglia: A neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. Journal of Cognitive Neuroscience 2005, 17(1):51-72.
54. Frank M.J., Moustafa A.A., Haughey H.M., Curran T., Hutchison K.E. Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(41):16311-16316.
55. Frank M.J., Seeberger L.C., O'Reilly R.C. By carrot or by stick: Cognitive reinforcement learning in parkinsonism. Science 2004, 306(5703):1940-1943.
56. Frey U., Schroeder H., Matthies H. Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Research 1990, 522(1):69-75.
57. Gabrieli J.D. Cognitive neuroscience of human memory. Annual Review of Psychology 1998, 49:87-115.
58. Gabrieli J.D., Stebbins G.T., Singh J., Willingham D.B., Goetz C.G. Intact mirror-tracing and impaired rotary-pursuit skill learning in patients with Huntington's disease: Evidence for dissociable memory systems in skill learning. Neuropsychology 1997, 11(2):272-281.
59. Gasbarri A., Packard M.G., Campana E., Pacitti C. Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Research Bulletin 1994, 33(4):445-452.
60. Gluck M.A., Shohamy D., Myers C. How do people solve the " weather prediction" task?: Individual variability in strategies for probabilistic category learning. Learning and Memory 2002, 9(6):408-418.
61. Graybiel A.M. The basal ganglia and chunking of action repertoires. Neurobiology of Learning and Memory 1998, 70(1/2):119-136.
62. Greene A.J., Spellman B.A., Dusek J.A., Eichenbaum H.B., Levy W.B. Relational learning with and without awareness: Transitive inference using nonverbal stimuli in humans. Memory and Cognition 2001, 29(6):893-902.
63. Haber S.N., Fudge J.L., McFarland N.R. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. Journal of Neuroscience 2000, 20(6):2369-2382.
64. Hannula D.E., Ryan J.D., Tranel D., Cohen N.J. Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia. Journal of Cognitive Neuroscience 2007, 19(10):1690-1705.
65. Hannula D.E., Tranel D., Cohen N.J. The long and the short of it: Relational memory impairments in amnesia, even at short lags. Journal of Neuroscience 2006, 26(32):8352-8359.
66. Hartley T., Burgess N. Complementary memory systems: Competition, cooperation and compensation. Trends in Neurosciences 2005, 28(4):169-170.
67. Hay J.F., Moscovitch M., Levine B. Dissociating habit and recollection: Evidence from Parkinson's disease, amnesia and focal lesion patients. Neuropsychologia 2002, 40(8):1324-1334.
68. Henke K. A model for memory systems based on processing modes rather than consciousness. Nature Reviews Neuroscience 2010, 11(7):523-532.
69. Hikosaka O., Miyashita K., Miyachi S., Sakai K., Lu X. Differential roles of the frontal cortex, basal ganglia, and cerebellum in visuomotor sequence learning. Neurobiology of Learning and Memory 1998, 70(1-2):137-149.
70. Joel D., Weiner I. The connections of the dopaminergic system with the striatum in rats and primates: An analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 2000, 96(3):451-474.
71. Jog M.S., Kubota Y., Connolly C.I., Hillegaart V., Graybiel A.M. Building neural representations of habits. Science 1999, 286(5445):1745-1749.
72. Jueptner M., Frith C.D., Brooks D.J., Frackowiak R.S., Passingham R.E. Anatomy of motor learning II. Subcortical structures and learning by trial and error. Journal of Neurophysiology 1997, 77(3):1325-1337.
73. Jueptner M., Weiller C. A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 1998, 121(Pt 8):1437-1449.
74. Kesner R.P., Bolland B.L., Dakis M. Memory for spatial locations, motor responses, and objects: Triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Experimental Brain Research 1993, 93(3):462-470.
75. Kish S.J., Shannak K., Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. New England Journal of Medicine 1988, 318(14):876-880.
76. Knecht S., Breitenstein C., Bushuven S., Wailke S., Kamping S., Floel A., et al. Levodopa: Faster and better word learning in normal humans. Annals of Neurology 2004, 56(1):20-26.
77. Knowlton B.J., Mangels J.A., Squire L.R. A neostriatal habit learning system in humans. Science 1996, 273(5280):1399-1402.
78. Knowlton B.J., Ramus S.J., Squire L.R. Intact artificial grammar learning in amnesia: Dissociation of classification learning and explicit memory for specific instances. Psychological Science 1992, 3(3):172-179.
79. Knowlton B.J., Squire L.R., Gluck M.A. Probabilistic classification learning in amnesia. Learning and Memory 1994, 1(2):106-120.
80. Laforce R., Doyon J. Distinct contribution of the striatum and cerebellum to motor learning. Brain and Cognition 2001, 45(2):189-211.
81. Lehericy S., Ducros M., Van de Moortele P.F., Francois C., Thivard L., Poupon C., et al. Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans. Annals of Neurology 2004, 55(4):522-529.
82. Lieberman M.D., Chang G.Y., Chiao J., Bookheimer S.Y., Knowlton B.J. An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. Journal of Cognitive Neuroscience 2004, 16(3):427-438.
83. Lisman J.E., Grace A.A. The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron 2005, 46(5):703-713.
84. Maddox W.T., Ashby F.G., Bohil C.J. Delayed feedback effects on rule-based and information-integration category learning. Journal of Experimental Psychology. Learning, Memory and Cognition 2003, 29(4):650-662.
85. McDonald R.J., White N.M. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience 1993, 107(1):3-22.
86. McDonald R.J., White N.M. Hippocampal and nonhippocampal contributions to place learning in rats. Behavioral Neuroscience 1995, 109(4):579-593.
87. Mega M.S., Cummings J.L. Frontal-subcortical circuits and neuropsychiatric disorders. Journal of Neuropsychiatry and Clinical Neurosciences 1994, 6(4):358-370.
88. Middleton F.A., Strick P.L. Basal ganglia output and cognition: Evidence from anatomical, behavioral, and clinical studies. Brain and Cognition 2000, 42(2):183-200.
89. Mishkin M., Malamut B., Bachevalier J. Memories and habits: Two neural systems. Neurobiology of learning and memory 1984, 65-77. Guilford Press, New York. G. Lynch, J.L. McGaugh, N. Weinberger (Eds.).
90. Mitchell J.A., Hall G. Caudate-putamen lesions in the rat may impair or potentiate maze learning depending upon availability of stimulus cues and relevance of response cues. Quarterly Journal of Experimental Psychology. B Comparative and Physiological Psychology 1988, 40(3):243-258.
91. Moody T.D., Bookheimer S.Y., Vanek Z., Knowlton B.J. An implicit learning task activates medial temporal lobe in patients with Parkinson's disease. Behavioral Neuroscience 2004, 118(2):438-442.
92. Moustafa A.A., Cohen M.X., Sherman S.J., Frank M.J. A role for dopamine in temporal decision making and reward maximization in parkinsonism. Journal of Neuroscience 2008, 28(47):12294-12304.
93. Myers C.E., Shohamy D., Gluck M.A., Grossman S., Kluger A., Ferris S., et al. Dissociating hippocampal versus basal ganglia contributions to learning and transfer. Journal of Cognitive Neuroscience 2003, 15(2):185-193.
94. Nissen M.J., Bullemer P. Attentional requirements of learning: Evidence from performance measures. Cognitive Psychology 1987, 19(1):1-32.
95. O'Doherty J.P., Dayan P., Friston K., Critchley H., Dolan R.J. Temporal difference models and reward-related learning in the human brain. Neuron 2003, 38(2):329-337.
96. O'Doherty J.P., Dayan P., Schultz J., Deichmann R., Friston K., Dolan R.J. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004, 304(5669):452-454.
97. Otmakhova N.A., Lisman J.E. D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. Journal of Neuroscience 1996, 16(23):7478-7486.
98. Owen A.M., Beksinska M., James M., Leigh P.N., Summers B.A., Marsden C.D., et al. Visuospatial memory deficits at different stages of Parkinson's disease. Neuropsychologia 1993, 31(7):627-644.
99. Packard M.G. Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proceedings of the National Academy of Sciences of the United States of America 1999, 96(22):12881-12886.
100. Packard M.G., Hirsh R., White N.M. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. Journal of Neuroscience 1989, 9(5):1465-1472.
101. Packard M.G., Knowlton B.J. Learning and memory functions of the basal ganglia. Annual Review of Neuroscience 2002, 25:563-593.
102. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65(1):65-72.
103. Pagnoni G., Zink C.F., Montague P.R., Berns G.S. Activity in human ventral striatum locked to errors of reward prediction. Nature Neuroscience 2002, 5(2):97-98.
104. Paller K.A., Wagner A.D. Observing the transformation of experience into memory. Trends Cognitive Science 2002, 6(2):93-102.
105. Peran P., Cherubini A., Assogna F., Piras F., Quattrocchi C., Peppe A., et al. Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain 2010, 133(11):3423-3433.
106. Poldrack R.A., Clark J., Pare-Blagoev E.J., Shohamy D., Moyano J.C., Myers C., et al. Interactive memory systems in the human brain. Nature 2001, 414(6863):546-550.
107. Poldrack R.A., Rodriguez P. How do memory systems interact? Evidence from human classification learning. Neurobiology of Learning and Memory 2004, 82(3):324-332.
108. Rabe A., Haddad R.K. Acquisition of two-way shuttle-box avoidance after selective hippocampal lesions. Physiology and Behavior 1969, 4(3):319-323.
109. Reber A.S. Implicit learning and tacit knowledge. Journal of Experimental Psychology: General 1989, 118(3):219-235.
110. Reber P.J., Knowlton B.J., Squire L.R. Dissociable properties of memory systems: Differences in the flexibility of declarative and nondeclarative knowledge. Behavioral Neuroscience 1996, 110(5):861-871.
111. Reber P.J., Squire L.R. Parallel brain systems for learning with and without awareness. Learning and Memory 1994, 1(4):217-229.
112. Reber P.J., Squire L.R. Encapsulation of implicit and explicit memory in sequence learning. Journal of Cognitive Neuroscience 1998, 10(2):248-263.
113. Reber P.J., Squire L.R. Intact learning of artificial grammars and intact category learning by patients with Parkinson's disease. Behavioral Neuroscience 1999, 113(2):235-242.
114. Redgrave P., Gurney K. The short-latency dopamine signal: A role in discovering novel actions?. Nature Review Neuroscience 2006, 7(12):967-975.
115. Redondo R.L., Morris R.G. Making memories last: The synaptic tagging and capture hypothesis. Nature Review Neuroscience 2011, 12(1):17-30.
116. Reynolds J.N., Wickens J.R. Dopamine-dependent plasticity of corticostriatal synapses. Neural Network 2002, 15(4-6):507-521.
117. Robbins T.W. Dissociating executive functions of the prefrontal cortex. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 1996, 351(1346):1463-1470.
118. Rodriguez P., Aron A., Poldrack R. Ventral-striatal/nucleus-accumbens sensitivity to prediction errors during classification learning. Human Brain Mapping 2006, 27(4):306-313.
119. Roesch M.R., Calu D.J., Schoenbaum G. Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nature Neuroscience 2007, 10(12):1615-1624.
120. Saint-Cyr J.A., Taylor A.E., Lang A.E. Procedural learning and neostriatal dysfunction in man. Brain 1988, 111(Pt 4):941-959.
121. Samson Y., Wu J.J., Friedman A.H., Davis J.N. Catecholaminergic innervation of the hippocampus in the cynomolgus monkey. Journal of Comparative Neurology 1990, 298(2):250-263.
122. Sanes J.N., Dimitrov B., Hallett M. Motor learning in patients with cerebellar dysfunction. Brain 1990, 113(Pt 1):103-120.
123. Schendan H.E., Searl M.M., Melrose R.J., Stern C.E. An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 2003, 37(6):1013-1025.
124. Schonberg T., Daw N.D., Joel D., O'Doherty J.P. Reinforcement learning signals in the human striatum distinguish learners from nonlearners during reward-based decision making. Journal of Neuroscience 2007, 27(47):12860-12867.
125. Schonberg T., O'Doherty J.P., Joel D., Inzelberg R., Segev Y., Daw N.D. Selective impairment of prediction error signaling in human dorsolateral but not ventral striatum in Parkinson's disease patients: Evidence from a model-based fMRI study. Neuroimage 2010, 49(1):772-781.
126. Schroeder J.P., Wingard J.C., Packard M.G. Post-training reversible inactivation of hippocampus reveals interference between memory systems. Hippocampus 2002, 12(2):280-284.
127. Schultz W. Dopamine neurons and their role in reward mechanisms. Current Opinion in Neurobiology 1997, 7(2):191-197.
128. Schultz W., Apicella P., Ljungberg T. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. Journal of Neuroscience 1993, 13(3):900-913.
129. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 1957, 20(1):11-21.
130. Seger C.A., Cincotta C.M. The roles of the caudate nucleus in human classification learning. Journal of Neuroscience 2005, 25(11):2941-2951.
131. Seger C.A., Dennison C.S., Lopez-Paniagua D., Peterson E.J., Roark A.A. Dissociating hippocampal and basal ganglia contributions to category learning using stimulus novelty and subjective judgments. Neuroimage 2011.
132. Seger C.A., Peterson E.J., Cincotta C.M., Lopez-Paniagua D., Anderson C.W. Dissociating the contributions of independent corticostriatal systems to visual categorization learning through the use of reinforcement learning modeling and Granger causality modeling. Neuroimage 2010, 50(2):644-656.
133. Seidler R.D., Purushotham A., Kim S.G., Ugurbil K., Willingham D., Ashe J. Neural correlates of encoding and expression in implicit sequence learning. Experimental Brain Research 2005, 165(1):114-124.
134. Seo M., Beigi M., Jahanshahi M., Averbeck B.B. Effects of dopamine medication on sequence learning with stochastic feedback in Parkinson's disease. Frontiers in Systems Neuroscience 2010, 4.
135. Seymour B., Daw N., Dayan P., Singer T., Dolan R. Differential encoding of losses and gains in the human striatum. Journal of Neuroscience 2007, 27(18):4826-4831.
136. Shohamy D., Adcock R.A. Dopamine and adaptive memory. Trends in Cognitive Science 2010, 14(10):464-472.
137. Shohamy D., Mihalakos P., Chin R., Thomas B., Wagner A.D., Tamminga C. Learning and generalization in schizophrenia: Effects of disease and antipsychotic drug treatment. Biological Psychiatry 2010, 67(10):926-932.
138. Shohamy D., Myers C.E., Geghman K.D., Sage J., Gluck M.A. L-dopa impairs learning, but spares generalization, in Parkinson's disease. Neuropsychologia 2006, 44(5):774-784.
139. Shohamy D., Myers C.E., Grossman S., Sage J., Gluck M.A. The role of dopamine in cognitive sequence learning: Evidence from Parkinson's disease. Behavioural Brain Research 2005, 156(2):191-199.
140. Shohamy D., Myers C.E., Grossman S., Sage J., Gluck M.A., Poldrack R.A. Cortico-striatal contributions to feedback-based learning: Converging data from neuroimaging and neuropsychology. Brain 2004, 127(Pt 4):851-859.
141. Shohamy D., Myers C.E., Onlaor S., Gluck M.A. Role of the basal ganglia in category learning: How do patients with Parkinson's disease learn?. Behavioral Neuroscience 2004, 118(4):676-686.
142. Shohamy D., Wagner A.D. Integrating memories in the human brain: Hippocampal-midbrain encoding of overlapping events. Neuron 2008, 60(2):378-389.
143. Smith J., Siegert R.J., McDowall J., Abernethy D. Preserved implicit learning on both the serial reaction time task and artificial grammar in patients with Parkinson's disease. Brain and Cognition 2001, 45(3):378-391.
144. Smith J.G., McDowall J. When artificial grammar acquisition in Parkinson's disease is impaired: The case of learning via trial-by-trial feedback. Brain Research 2006, 1067(1):216-228.
145. Squire L.R. Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory 2004, 82(3):171-177.
146. Squire L.R., Zola S.M. Structure and function of declarative and nondeclarative memory systems. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(24):13515-13522.
147. Swainson R., Rogers R.D., Sahakian B.J., Summers B.A., Polkey C.E., Robbins T.W. Probabilistic learning and reversal deficits in patients with Parkinson's disease or frontal or temporal lobe lesions: Possible adverse effects of dopaminergic medication. Neuropsychologia 2000, 38(5):596-612.
148. Takahashi H., Kato M., Takano H., Arakawa R., Okumura M., Otsuka T., et al. Differential contributions of prefrontal and hippocampal dopamine D(1) and D(2) receptors in human cognitive functions. Journal of Neuroscience 2008, 28(46):12032-12038.
149. Tremblay L., Hollerman J.R., Schultz W. Modifications of reward expectation-related neuronal activity during learning in primate striatum. Journal of Neurophysiology 1998, 80(2):964-977.
150. Tricomi E., Balleine B.W., O'Doherty J.P. A specific role for posterior dorsolateral striatum in human habit learning. European Journal of Neuroscience 2009, 29(11):2225-2232.
151. Tricomi E., Delgado M., Fiez J. Modulation of caudate activity by action contingency. Neuron 2004, 41(2):281-292.
152. Uncapher M.R., Rugg M.D. Fractionation of the component processes underlying successful episodic encoding: A combined fMRI and divided-attention study. Journal of Cognitive Neuroscience 2008, 20(2):240-254.
153. Valentin V.V., Dickinson A., O'Doherty J.P. Determining the neural substrates of goal-directed learning in the human brain. Journal of Neuroscience 2007, 27(15):4019-4026.
154. Voermans N.C., Petersson K.M., Daudey L., Weber B., Van Spaendonck K.P., Kremer H.P., et al. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 2004, 43(3):427-435.
155. Vriezen E.R., Moscovitch M. Memory for temporal order and conditional associative-learning in patients with Parkinson's disease. Neuropsychologia 1990, 28(12):1283-1293.
156. Waelti P., Dickinson A., Schultz W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 2001, 412(6842):43-48.
157. White N.M. Mnemonic functions of the basal ganglia. Current Opinion in Neurobiology 1997, 7(2):164-169.
158. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning and Memory 2002, 77(2):125-184.
159. Whittington C.J., Podd J., Kan M.M. Recognition memory impairment in Parkinson's disease: Power and meta-analyses. Neuropsychology 2000, 14(2):233-246.
160. Whittington C.J., Podd J., Stewart-Williams S. Memory deficits in Parkinson's disease. Journal of Clinical and Experimental Neuropsychology 2006, 28(5):738-754.
161. Wilkinson L., Khan Z., Jahanshahi M. The role of the basal ganglia and its cortical connections in sequence learning: Evidence from implicit and explicit sequence learning in Parkinson's disease. Neuropsychologia 2009, 47(12):2564-2573.
162. Willingham D.B., Salidis J., Gabrieli J.D. Direct comparison of neural systems mediating conscious and unconscious skill learning. Journal of Neurophysiology 2002, 88(3):1451-1460.
163. Wirth S., Yanike M., Frank L.M., Smith A.C., Brown E.N., Suzuki W.A. Single neurons in the monkey hippocampus and learning of new associations. Science 2003, 300(5625):1578-1581.
164. Wittmann B.C., Bunzeck N., Dolan R.J., Duzel E. Anticipation of novelty recruits reward system and hippocampus while promoting recollection. Neuroimage 2007, 38(1):194-202.
165. Wittmann B.C., Schott B.H., Guderian S., Frey J.U., Heinze H.J., Duzel E. Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron 2005, 45(3):459-467.
166. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nature Reviews Neuroscience 2006, 7:464-476.
167. Yin H.H., Knowlton B.J., Balleine B.W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. European Journal of Neuroscience 2004, 19(1):181-189.
168. Yin H.H., Knowlton B.J., Balleine B.W. Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. European Journal of Neuroscience 2005, 22(2):505-512.
169. Yin H.H., Knowlton B.J., Balleine B.W. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behavioral Brain Research 2006, 166(2):189-196.