The striatum and probabilistic implicit sequence learning

Brain Research

Volumn 1137, Issue 1, 2007, Pages 117-130

  Wilkinson, Leonora ^a   Jahanshahi, Marjan ^a  

^a NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

Author keywords

Basal ganglia; Implicit learning; Parkinson's disease; Process dissociation procedure; Sequence learning; Serial reaction time task

Indexed keywords

ADULT; AGED; ARTICLE; BASAL GANGLION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; HUMAN; LEARNING; MALE; PARKINSON DISEASE; PRIORITY JOURNAL; RECOGNITION; TEMPORAL LOBE;

AGED; ANALYSIS OF VARIANCE; AWARENESS; CASE-CONTROL STUDIES; CORPUS STRIATUM; FEMALE; HUMANS; MALE; MIDDLE AGED; MODELS, STATISTICAL; NEUROPSYCHOLOGICAL TESTS; PARKINSON DISEASE; REACTION TIME; RECOGNITION (PSYCHOLOGY); SERIAL LEARNING;

EID: 33846924103     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.12.051     Document Type: Article

References (94)

1. Aron A.R., Shohamy D., Myers C., Gluck M.A., and Poldrack R.A. Human midbrain sensitivity to cognitive feedback and uncertainty during classification learning. J. Neurophysiol. 92 (2004) 1144-1152
2. Aron A.R., Gluck M.A., and Poldrack R.A. Long-term test-retest reliability of functional MRI in a classification learning task. NeuroImage 29 (2006) 1000-1006
3. Beck, A.T., Steer, R.A., Brown, G.K., 1996. Manual for the Beck Depression Inventory. Psychological Corporation, San Antonio, TX.
4. Beiser D.G., and Houk J.C. Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. J. Neurophysiol. 79 6 (1998) 3168-3188
5. Brooks D.J. Functional imaging studies on dopamine and motor control. J. Neural Trans. 108 11 (2001) 1283-1298
6. Brown R.G., and Marsden C.D. Dual task-performance and processing resources in normal subjects and patients with Parkinson's-disease. Brain 114 (1991) 215-231
7. Brown R.G., Jahanshahi M., and Marsden C.D. The execution of bimanual movements in patients with Parkinson, Huntington and cerebellar disease. J. Neurol., Neurosurg. Psychiatry 56 3 (1993) 295-297
8. Brown R.G., Redondo-Verge L., Chacon J.R., Lucas M.L., and Channon S. Dissociation between intentional and incidental sequence learning in Huntington's disease. Brain 124 (2001) 2188-2202
9. Brown R.G., Jahanshahi M., Limousin-Dowsey P., Thomas D., Quinn N., and Rothwell J.C. Pallidotomy and incidental sequence learning in Parkinson's disease. NeuroReport 14 1 (2003) 1-4
10. Butters N., Wolfe J., Martone M., Granholm E., and Cermak L.S. Memory disorders associated with Huntington's disease-Verbal recall, verbal recognition and procedural memory. Neuropsychologia 23 6 (1985) 729-743
11. Carbon M., Ghilardi M.F., Feigin A., Fukuda M., Silvestri G., Mentis M.J., et al. Learning networks in health and Parkinson's disease: reproducibility and treatment effects. Hum. Brain Mapp. 19 3 (2003) 197-211
12. Cohen N.J., and Squire L.R. Preserved learning and retention of pattern analysing skill in amnesia: dissociation of knowing how and knowing that. Science 210 (1980) 109-207
13. Cools R., Barker R.A., Sahakian B.J., and Robbins T.W. Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. Cereb. Cortex 11 12 (2001) 1136-1143
14. Cools R., Barker R.A., Sahakian B.J., and Robbins T.W. l-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson's disease. Neuropsychologia 41 11 (2003) 1431-1441
15. Cools R., Altamirano L., and D'Esposito M. Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 44 10 (2006) 1663-1673
16. Curran T. Effects of ageing on implicit sequence learning: accounting for sequence structure and explicit knowledge. Psychol. Res. 60 (1997) 24-41
17. Destrebecqz A., and Cleeremans A. Can sequence learning be implicit? New evidence with the process dissociation procedure. Psychon. Bull. Rev. 8 (2001) 343-350
18. Destrebecqz A., and Cleeremans A. Temporal effects in sequence learning. In: Jiménez L. (Ed). Attention and Implicit Learning (2003), John Benjamins, Amsterdam 181-213
19. Doyon J., Owen A.M., Petrides M., Sziklas V., and Evans A.C. Functional anatomy of visuomotor skill learning in human participants examined with positron emission tomography. Eur. J. Neurosci. 8 4 (1996) 637-648
20. Doyon J., Ganreau 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 repeated visuomotor sequence. Brain Cogn. 34 (1997) 218-245
21. Doyon J., Laforce R., Bouchard J.P., Gandreau 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 36 (1998) 625-641
22. Ferraro F.R., Balota D.A., and Connor L.T. Implicit memory and the formation of new associations in nondemented Parkinson's disease individuals and individuals with senile dementia of the Alzheimer type: a serial reaction time (SRT) investigation. Brain Cogn. 21 (1993) 163-180
23. Fernandez-Ruiz J., Wang J., Aigner T.G., and Mishkin N. Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc. Natl. Acad. Sci. U. S. A. 98 7 (2001) 4196-4201
24. Field A.P. Discovering Statistics Using SPSS. 2nd ed. (2005), Sage, London
25. Filoteo J.V., Maddox W.T., and Davis J. Probabilistic category learning in patients with amnesia, Huntington's disease, or Parkinson's disease: the role of the hippocampus and basal ganglia. J. Cogn. (1998) 108
26. Folstein M., Folstein S., and McHugh P. "Mini-mental state": A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12 (1975) 189-198
27. Frank M.J., Seeberger L.C., and O'reilly R.C. By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306 5703 (2004) 1940-1943
28. Frank M.J. Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J. Cogn. Neurosci. 17 (2005) 51-72
29. Gotham A.M., Brown R.G., and Marsden C.D. 'Frontal' cognitive function in patients with Parkinson's disease 'on' and 'off' levodopa. Brain 111 (1988) 299-321
30. Grafton S.T., Hazeltine E., and Ivry R. Functional mapping of sequence learning in normal humans. J. Cogn. Neurosci. 7 (1995) 497-510
31. Hazeltine E., Grafton S.T., and Ivry R. Attention and stimulus characteristics determine the locus of motor-sequence encoding-a PET study. Brain 120 (1997) 123-140
32. Helmuth L.L., Mayr U., and Daum I. Sequence learning in Parkinson's disease: a comparison of spatial-attention and number-response sequences. Neuropsychologia 38 11 (2000) 1443-1451
33. Hoehn M.M., and Yahr M.D. Parkinsonism: onset, progression and mortality. Neurology 7 17 (1967) 427-442
34. Honda M., Deiber M.P., Ibáñez V., Pascual-Leone A., Zhuang P., and Hallett M. Dynamic cortical involvement in implicit and explicit motor sequence learning: a PET study. Brain 121 (1998) 2159-2173
35. Huang Y.Z., and Rothwell J.C. The effect of short-duration bursts of high-frequency, low-intensity transcranial magnetic stimulation on the human motor cortex. Clin. Neurophysiol. 115 5 (2004) 1069-1075
36. Hughes A.J., Daniel S.E., Kilford L., and Lees A.J. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J. Neurol. Neurosurg. Psychiat. 55 (1992) 181-184
37. Jackson G.M., Jackson S.R., Harrison J., Henderson L., and Kennard C. Serial reaction time learning and Parkinson's disease: evidence for a procedural learning defect. Neuropsychology 33 (1995) 577-593
38. Jacoby L.L. A process dissociation framework: separating automatic from intentional uses of memory. J. Mem. Lang. 30 (1991) 513-541
39. Jacoby L.L., Toth J.P., and Yonelinas A.P. Separating conscious and unconscious influences of memory: measuring recollection. J. Exp. Psychol. Gen. 122 (1993) 139-154
40. Jacoby L.L., Woloshyn V., and Kelley C.M. Becoming famous without being recognized: unconscious influences of memory produced by dividing attention. J. Exp. Psychol. Gen. 118 (1989) 115-125
41. Jenkins I.H., Brooks D.J., Nixon P.D., Frackowiak R.S.J., and Passingham R.E. Motor sequence learning-a study with positron emission tomography. J. Neurosci. 14 6 (1994) 3775-3790
42. Jog M.S., Kubota Y., Connolly C.I., Hillegaart V., and Graybiel A.M. Building neural representations of habits. Science 286 5445 (1999) 1745-1749
43. Kelly S., Jahanshahi M., and Dirnberger G. Learning of hybrid and ambiguous sequences by patients with Parkinson's disease. Neuropsychologia 42 10 (2004) 1350-1357
44. Knopman D.S., and Nissen M.J. Procedural learning is impaired in Huntington's disease-evidence from the serial reaction-time-task. Neuropsychologia 29 3 (1991) 245-254
45. Knowlton B.J., Mangels J.A., and Squire L.R. A neostriatal habit learning system in humans. Science 273 5280 (1996) 1399-1402
46. Knowlton B.J., Squire L.R., Paulsen J.S., Swerdlow N.R., Swenson M., and Butters N. Dissociations within nondeclarative memory in Huntington's disease. Neuropsychology 10 4 (1996) 538-548
47. Lange K.W., Robbins T.W., Marsden C.D., James M., Owen A.M., and Paul G.M. l-dopa withdrawal in Parkinson's disease selectively impairs cognitive performance in tests sensitive to frontal lobe dysfunction. Psychopharmacology 107 (1992) 394-404
48. McDonald R.J., and White N.M. A triple dissociation of memory-systems-hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 107 1 (1993) 3-22
49. Merikle P.M. Perception without awareness: critical issues. Am. Psychol. 47 (1992) 792-795
50. Merikle P.M., Smilek D., and Eastwood J.D. Perception without awareness: perspectives from cognitive psychology. Cognition 79 (2001) 115-134
51. Monchi O., Petrides M., Doyon J., Postuma R.B., Worsley K., and Daqher A. Neural bases of set-shifting deficits in Parkinson's disease. J. Neurosci. 24 3 (2004) 702-710
52. Nissen M.J., and Bullemer P. Attentional requirements of learning: evidence from performance measures. Cogn. Psychol. 19 (1987) 1-32
53. Norman D.A., and Shallice T. Attention in action. Willed and automatic control of behaviour. In: Davidson R.J., Schwartz G.E., and Shapiro D. (Eds). Consciousness and Self-regulation vol. 4 (1986), Plenum Press, New York
54. Packard M.G., Hirsh R., and White N.M. Differential-effects of fornix and caudate-nucleus lesions on 2 radial maze tasks-evidence for multiple memory-systems. J. Neurosci. 9 (1989) 1465-1472
55. Packard M.G., and McGaugh J.L. Double dissociation of fornix and caudate-nucleus lesions on acquisition of 2 water maze tasks-further evidence for multiple memory-systems. Behav. Neurosci. 106 3 (1992) 439-446
56. Pascual-Leone A., Grafman J., Clark K., Stewart M., Massaquios S., and Hallett M. Procedural learning in Parkinson's disease and cerebellar degeneration. Ann. Neurol. 34 (1993) 594-602
57. Peigneux P., Maquet P., Meulemans T., Destrebecqz A., Laureys S., Degueldre C., et al. Striatum forever, despite sequence learning variability: a random effect analysis of PET data. Hum. Brain Mapp. 10 4 (2000) 179-194
58. Perruchet P., and Amorim M.A. Conscious knowledge and changes in performance in sequence learning: evidence against dissociation. J. Exper. Psychol., Learn., Mem., Cogn. 18 (1992) 785-800
59. Pessiglione M., Seymour B., Flandin G., Dolan R.J., and Frith C.D. Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442 7106 (2006) 1042-1045
60. Poewe W., Berger W., Benke T., and Schelosky L. High-speed memory scanning in Parkinsons-disease-adverse-effects of levodopa. Ann. Neurol. 29 6 (1991) 670-673
61. Poldrack R.A., Prabhakaran V., Seger C.A., and Gabrieli J.D.E. Striatal activation during acquisition of a cognitive skill. Neuropsychology 13 4 (1999) 564-574
62. 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 414 6863 (2001) 546-550
63. Rauch S.L., Savage C.R., Brown H.D., Curran T., Alpert N.M., Kendrick A., et al. A PET investigation of implicit and explicit sequence learning. Hum. Brain Mapp. 3 4 (1995) 271-286
64. Rauch S.L., Whalen P.J., Savage C.R., Curran T., Kendrick A., Brown H.D., et al. Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Hum. Brain Mapp. 5 2 (1997) 124-132
65. Reber P.J., and Squire L.R. Parallel brain systems for learning with and without awareness. Learn. Mem. 1 (1994) 217-229
66. Reber P.J., and Squire L.R. Encapsulation of implicit and explicit memory in sequence learning. J. Cogn. Neurosci. 10 2 (1998) 248-263
67. Reed J., and Johnson P. Assessing implicit learning with indirect tests: determining what is learned about sequence structure. J. Exper. Psychol., Learn., Mem., Cogn. 20 (1994) 585-594
68. Sage J.R., Anagnostaras S.G., Mitchell S., Bronstein J.M., De Salles A., Masterman D., et al. Analysis of probabilistic classification learning in patients with Parkinson's disease before and after pallidotomy surgery. Learn. Mem. 10 3 (2003) 226-236
69. Schultz W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80 1 (1998) 1-27
70. Schultz W. Multiple reward signals in the brain. Nat. Rev., Neurosci. 1 3 (2000) 199-207
71. Schultz W., Tremblay L., and Hollerman J.R. Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb. Cortex 10 3 (2000) 272-283
72. Seger C.A., and Cinotta M. The roles of the caudate nucleus in human classification learning. J. Neurosci. 25 11 (2005) 2941-2951
73. Shanks D.R., and Channon S. Effects of a secondary task on "implicit" sequence learning or performance?. Psychol. Res. 66 (2002) 99-109
74. Shanks D.R., Channon S., Wilkinson L., and Curran H.V. Disruption of sequential priming in organic and pharmacological amnesia: a role for the medial temporal lobes in implicit contextual learning. J. Neuro-psychopharmacol. 31 (2006) 1768-1776
75. Shanks D.R., and Johnstone T. Implicit knowledge in sequential learning tasks. In: Stadler M.A., and Frensch P.A. (Eds). Handbook of Implicit Learning (1998), Sage, Thousand Oaks, CA 533-572
76. Shanks D.R., and Johnstone T. Evaluating the relationship between explicit and implicit knowledge in a sequential reaction time task. J. Exper. Psychol., Learn., Mem., Cogn. 25 (1999) 1435-1451
77. Shanks D.R., and Perruchet P. Dissociation between priming and recognition in the expression of sequential knowledge. Psychon. Bull. Rev. 9 (2002) 362-367
78. Shanks D.R., and St. John M.F. Characteristics of dissociable human learning systems. Behav. Brain Sci. 17 (1994) 367-447
79. Shanks D.R., Wilkinson L., and Channon S. Relationship between priming and recognition in deterministic and probabilistic sequence learning. J. Exper. Psychol., Learn., Mem., Cogn. 29 (2003) 248-261
80. Shohamy D., Myers C.E., Onlaor S., and Gluck M.A. Role of the basal ganglia in category learning: how do patients with Parkinson's disease learn?. Behav. Neurosci. 118 (2004) 676-686
81. Shohamy D., Myers C.E., Grossman S., Sage J., Gluck M.A., and Poldrack R.A. Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. Brain 127 (2004) 851-859
82. Shohamy D., Myers C.E., Grossman S., Sage J., and Gluck M.A. The role of dopamine in cognitive sequence learning: evidence from Parkinson's disease. Behav. Brain Res. 156 2 (2005) 191-199
83. Shin J.C., and Ivry R.B. Spatial and temporal sequence learning in patients with Parkinson's disease or cerebellar lesions. J. Cogn. Neurosci. 15 8 (2003) 1232-1243
84. Siegert R.J., Taylor K.D., Weatherall M., and Albernethy D.A. Is implicit sequence learning impaired in PD? A meta-analysis. Neuropsychology 20 4 (2006) 490-495
85. Smith J., Siegert R.J., and McDowall J. Preserved implicit learning on both the serial reaction time task and artificial grammar in patients with Parkinson's disease. Brain Cogn. 45 3 (2001) 378-391
86. Sommer M., Grafman J., Clark K., and Hallett M. Learning in Parkinson's disease: eye blink conditioning, declarative learning, and procedural learning. J. Neurol., Neurosurg. Psychiatry 67 1 (1999) 27-34
87. Soliveri P., Brown R.G., Jahanshahi M., Caraceni R., and Marsden C.D. Learning manual pursuit tracking skills in patients with Parkinson's disease. Brain 120 (1997) 1325-1337
88. Westwater H., McDowall J., Siegert R., Mossman S., and Abernethy D. Implicit learning in Parkinson's disease: evidence from a verbal version of the serial reaction time task. J. Clin. Exp. Neuropsychol. 20 (1998) 413-418
89. Werheid K., Ziessler M., Nattkemper D., and von Cramon D.Y. Sequence learning in Parkinson's disease: the effect of spatial stimulus-response compatibility. Brain Cogn. 52 2 (2003) 239-249
90. Wilkinson L., and Shanks D.R. Intentional control and implicit sequence learning. J. Exper. Psychol., Learn., Mem., Cogn. 30 2 (2004) 354-369
91. Willingham D.B., Greely T., and Bardone A.M. Dissociation in a serial response time task using a recognition measure: comment on Perruchet and Amorim (1992). J. Exper. Psychol., Learn. Mem., Cogn. 19 6 (1993) 1424-1430
92. Willingham D.B., and Koroshetz W.J. Evidence for dissociable motor skills in Huntington's disease individuals. Psychobiology 21 (1993) 173-182
93. Willingham D.B., Salidis J., and Gabrieli J.D.E. Direct comparison of neural systems mediating conscious and unconscious skill learning. J. Neurophysiol. 88 (2002) 1451-1460
94. Witt K., Nuhsman A., and Deuschl G. Dissociation of habit-learning in Parkinson's and cerebellar disease. J. Cogn. Neurosci. 14 3 (2002) 493-499