Differential Effects of Parkinson's Disease and Dopamine Replacement on Memory Encoding and Retrieval

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  MacDonald, Alex A ^a   Seergobin, Ken N ^a   Owen, Adrian M ^a   Tamjeedi, Ruzbeh ^b   Monchi, Oury ^c,d   Ganjavi, Hooman ^a   MacDonald, Penny A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c CENTRE DE RECHERCHE   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; LEVODOPA; PRAMIPEXOLE;

ADULT; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; HUMAN; LEARNING TEST; MEMORY; MEMORY ENCODING; MEMORY RETRIEVAL; MENTAL PERFORMANCE; PARKINSON DISEASE;

CASE-CONTROL STUDIES; DOPAMINE; HUMANS; MEMORY; MIDDLE AGED; PARKINSON DISEASE; VERBAL LEARNING;

EID: 84884658605     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074044     Document Type: Article

References (95)

1. Kish SJ, Shannak K, Hornykiewicz O, (1988) Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 318: 876-880.
2. Lang AE, Blair RD, (1984) Parkinson's disease in 1984: an update. Can Med Assoc J 131: 1031-1037.
3. Aarsland D, Zaccai J, Brayne C, (2005) A systematic review of prevalence studies of dementia in Parkinson's disease. Mov Disord 20: 1255-1263.
4. Macdonald PA, Macdonald AA, Seergobin KN, Tamjeedi R, Ganjavi H, et al. (2011) The effect of dopamine therapy on ventral and dorsal striatum-mediated cognition in Parkinson's disease: support from functional MRI. Brain 134: 1447-1463.
5. Cools R, Lewis SJ, Clark L, Barker RA, Robbins TW, (2007) L-DOPA disrupts activity in the nucleus accumbens during reversal learning in Parkinson's disease. Neuropsychopharmacology 32: 180-189.
6. Macdonald AA, Monchi O, Seergobin KN, Ganjavi H, Tamjeedi R, et al. (2013) Parkinson's disease duration determines effect of dopaminergic therapy on ventral striatum function. Mov Disord 28: 153-160.
7. Weiermann B, Stephan MA, Kaelin-Lang A, Meier B, (2010) Is there a recognition memory deficit in Parkinson's disease? Evidence from estimates of recollection and familiarity. Int J Neurosci 120: 211-216.
8. Taylor AE, Saint-Cyr JA, Lang AE, (1990) Memory and learning in early Parkinson's disease: evidence for a "frontal lobe syndrome". Brain Cogn 13: 211-232.
9. Davidson PS, Anaki D, Saint-Cyr JA, Chow TW, Moscovitch M, (2006) Exploring the recognition memory deficit in Parkinson's disease: estimates of recollection versus familiarity. Brain 129: 1768-1779.
10. Edelstyn NM, Shepherd TA, Mayes AR, Sherman SM, Ellis SJ, (2010) Effect of disease severity and dopaminergic medication on recollection and familiarity in patients with idiopathic nondementing Parkinson's. Neuropsychologia 48: 1367-1375.
11. Bronnick K, Alves G, Aarsland D, Tysnes OB, Larsen JP, (2011) Verbal memory in drug-naive, newly diagnosed Parkinson's disease. The retrieval deficit hypothesis revisited. Neuropsychology 25: 114-124.
12. Cohn M, Moscovitch M, Davidson PS, (2010) Double dissociation between familiarity and recollection in Parkinson's disease as a function of encoding tasks. Neuropsychologia 48: 4142-4147.
13. Craik FI, Govoni R, Naveh-Benjamin M, Anderson ND, (1996) The effects of divided attention on encoding and retrieval processes in human memory. J Exp Psychol Gen 125: 159-180.
14. Mayes AR, Roberts N, (2001) Theories of episodic memory. Philos Trans R Soc Lond B Biol Sci 356: 1395-1408.
15. Moscovitch M, (1992) Memory and Working-with-Memory - a Component Process Model Based on Modules and Central Systems. Journal of Cognitive Neuroscience 4: 257-267.
16. Huijbers W, Schultz AP, Vannini P, McLaren DG, Wigman SE, et al. (2013) The Encoding/Retrieval Flip: Interactions between Memory Performance and Memory Stage and Relationship to Intrinsic Cortical Networks. J Cogn Neurosci 25: 1163-1179.
17. Shrager Y, Kirwan CB, Squire LR, (2008) Activity in both hippocampus and perirhinal cortex predicts the memory strength of subsequently remembered information. Neuron 59: 547-553.
18. Daselaar SM, Prince SE, Cabeza R, (2004) When less means more: deactivations during encoding that predict subsequent memory. Neuroimage 23: 921-927.
19. Otten LJ, Rugg MD, (2001) Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cereb Cortex 11: 1150-1160.
20. Kim H, (2010) Dissociating the roles of the default-mode, dorsal, and ventral networks in episodic memory retrieval. Neuroimage 50: 1648-1657.
21. Hutchinson JB, Uncapher MR, Wagner AD, (2009) Posterior parietal cortex and episodic retrieval: convergent and divergent effects of attention and memory. Learn Mem 16: 343-356.
22. Konishi S, Wheeler ME, Donaldson DI, Buckner RL, (2000) Neural correlates of episodic retrieval success. Neuroimage 12: 276-286.
23. Schacter DL, Buckner RL, Koutstaal W, Dale AM, Rosen BR, (1997) Late onset of anterior prefrontal activity during true and false recognition: an event-related fMRI study. Neuroimage 6: 259-269.
24. Drag LL, Bieliauskas LA, Kaszniak AW, Bohnen NI, Glisky EL, (2009) Source memory and frontal functioning in Parkinson's disease. J Int Neuropsychol Soc 15: 399-406.
25. Defer GL, Widner H, Marie RM, Remy P, Levivier M, (1999) Core assessment program for surgical interventional therapies in Parkinson's disease (CAPSIT-PD). Mov Disord 14: 572-584.
26. Hughes AJ, Daniel SE, Kilford L, Lees AJ, (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55: 181-184.
27. Declaration of Helsinki. Law Med Health Care 19: 264-265.
28. Evans AH, Katzenschlager R, Paviour D, O'Sullivan JD, Appel S, et al. (2004) Punding in Parkinson's disease: its relation to the dopamine dysregulation syndrome. Mov Disord 19: 397-405.
29. Benjamin AS, Tullis J, (2010) What makes distributed practice effective? Cogn Psychol 61: 228-247.
30. de Zubicaray GI, McMahon KL, Eastburn MM, Finnigan S, Humphreys MS, (2005) FMRI evidence of word frequency and strength effects during episodic memory encoding. Cognitive Brain Research 22: 439-450.
31. Vakil E, Greenstein Y, Blachstein H, (2010) Normative data for composite scores for children and adults derived from the Rey Auditory Verbal Learning Test. Clin Neuropsychol 24: 662-677.
32. Lezak MD (2004) Neuropsychological assessment. New York: Oxford University Press. xiv, 1016 p.
33. Mitrushina MN, Boone KB, D'Elia L (1999) Handbook of normative data for neuropsychological assessment. New York: Oxford University Press. xxii, 531 p.
34. Wixted JT, Ebbesen EB, (1991) On the Form of Forgetting. Psychological Science 2: 409-415.
35. Yonelinas AP, Kroll NE, Quamme JR, Lazzara MM, Sauve MJ, et al. (2002) Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat Neurosci 5: 1236-1241.
36. Macmillan NA, Creelman CD (2005) Detection theory: a user's guide. Mahwah, N.J.; London: Lawrence Erlbaum Associates. xix, 492 p.
37. Algarabel S, Rodriguez LA, Escudero J, Fuentes M, Peset V, et al. (2010) Recognition by familiarity is preserved in Parkinson's without dementia and Lewy-Body disease. Neuropsychology 24: 599-607.
38. van Eimeren T, Ballanger B, Pellecchia G, Miyasaki JM, Lang AE, et al. (2009) Dopamine agonists diminish value sensitivity of the orbitofrontal cortex: a trigger for pathological gambling in Parkinson's disease? Neuropsychopharmacology 34: 2758-2766.
39. Argyelan M, Carbon M, Ghilardi MF, Feigin A, Mattis P, et al. (2008) Dopaminergic suppression of brain deactivation responses during sequence learning. J Neurosci 28: 10687-10695.
40. Cools R, (2006) Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 30: 1-23.
41. Lisman JE, Grace AA, (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46: 703-713.
42. Adcock RA, Thangavel A, Whitfield-Gabrieli S, Knutson B, Gabrieli JD, (2006) Reward-motivated learning: mesolimbic activation precedes memory formation. Neuron 50: 507-517.
43. Schultz W, (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27.
44. Bayer HM, Glimcher PW, (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47: 129-141.
45. Knecht S, Breitenstein C, Bushuven S, Wailke S, Kamping S, et al. (2004) Levodopa: faster and better word learning in normal humans. Ann Neurol 56: 20-26.
46. Floel A, Garraux G, Xu B, Breitenstein C, Knecht S, et al. (2008) Levodopa increases memory encoding and dopamine release in the striatum in the elderly. Neurobiol Aging 29: 267-279.
47. Atallah HE, Lopez-Paniagua D, Rudy JW, O'Reilly RC, (2007) Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nat Neurosci 10: 126-131.
48. Vakil E, Blachstein H, (1993) Rey Auditory-Verbal Learning Test: structure analysis. J Clin Psychol 49: 883-890.
49. Woodard JL, Dunlosky JA, Salthouse TA, (1999) Task decomposition analysis of intertrial free recall performance on the Rey Auditory Verbal Learning Test in normal aging and Alzheimer's disease. J Clin Exp Neuropsychol 21: 666-676.
50. Crawford JR, Stewart LE, Moore JW, (1989) Demonstration of savings on the AVLT and development of a parallel form. J Clin Exp Neuropsychol 11: 975-981.
51. Pollak Y, Kahana-Vax G, Hoofien D, (2008) Retrieval processes in adults with ADHD: a RAVLT study. Dev Neuropsychol 33: 62-73.
52. Beato R, Levy R, Pillon B, Vidal C, du Montcel ST, et al. (2008) Working memory in Parkinson's disease patients: clinical features and response to levodopa. Arq Neuropsiquiatr 66: 147-151.
53. Mattay VS, Tessitore A, Callicott JH, Bertolino A, Goldberg TE, et al. (2002) Dopaminergic modulation of cortical function in patients with Parkinson's disease. Ann Neurol 51: 156-164.
54. Mollion H, Ventre-Dominey J, Dominey PF, Broussolle E, (2003) Dissociable effects of dopaminergic therapy on spatial versus non-spatial working memory in Parkinson's disease. Neuropsychologia 41: 1442-1451.
55. Lange KW, Robbins TW, Marsden CD, James M, Owen AM, et al. (1992) L-dopa withdrawal in Parkinson's disease selectively impairs cognitive performance in tests sensitive to frontal lobe dysfunction. Psychopharmacology (Berl) 107: 394-404.
56. Slabosz A, Lewis SJ, Smigasiewicz K, Szymura B, Barker RA, et al. (2006) The role of learned irrelevance in attentional set-shifting impairments in Parkinson's disease. Neuropsychology 20: 578-588.
57. Lewis SJ, Slabosz A, Robbins TW, Barker RA, Owen AM, (2005) Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson's disease. Neuropsychologia 43: 823-832.
58. Costa A, Peppe A, Dell'Agnello G, Carlesimo GA, Murri L, et al. (2003) Dopaminergic modulation of visual-spatial working memory in Parkinson's disease. Dement Geriatr Cogn Disord 15: 55-66.
59. Costa A, Peppe A, Dell'Agnello G, Caltagirone C, Carlesimo GA, (2009) Dopamine and cognitive functioning in de novo subjects with Parkinson's disease: effects of pramipexole and pergolide on working memory. Neuropsychologia 47: 1374-1381.
60. Cools R, Miyakawa A, Sheridan M, D'Esposito M, (2010) Enhanced frontal function in Parkinson's disease. Brain 133: 225-233.
61. Mehta MA, Swainson R, Ogilvie AD, Sahakian J, Robbins TW, (2001) Improved short-term spatial memory but impaired reversal learning following the dopamine D(2) agonist bromocriptine in human volunteers. Psychopharmacology (Berl) 159: 10-20.
62. Kimberg DY, D'Esposito M, Farah MJ, (1997) Effects of bromocriptine on human subjects depend on working memory capacity. Neuroreport 8: 3581-3585.
63. Kimberg DY, D'Esposito M, (2003) Cognitive effects of the dopamine receptor agonist pergolide. Neuropsychologia 41: 1020-1027.
64. Muller U, von Cramon DY, Pollmann S, (1998) D1- versus D2-receptor modulation of visuospatial working memory in humans. J Neurosci 18: 2720-2728.
65. Luciana M, Depue RA, Arbisi P, Leon A, (1992) Facilitation of working memory in human by a D2 dopamine receptor agonist. Journal of Cognitive Neuroscience 4: 58-68.
66. Luciana M, Collins PF, (1997) Dopamine modulates working memory for spatial but not object cues in normal humans. Journal of Cognitive Neuroscience 9: 330-347.
67. Lee J, Zhu WM, Stanic D, Finkelstein DI, Horne MH, et al. (2008) Sprouting of dopamine terminals and altered dopamine release and uptake in Parkinsonian dyskinaesia. Brain 131: 1574-1587.
68. Feigin A, Ghilardi MF, Carbon M, Edwards C, Fukuda M, et al. (2003) Effects of levodopa on motor sequence learning in Parkinson's disease. Neurology 60: 1744-1749.
69. Jahanshahi M, Wilkinson L, Gahir H, Dharminda A, Lagnado DA, (2010) Medication impairs probabilistic classification learning in Parkinson's disease. Neuropsychologia 48: 1096-1103.
70. Seo M, Beigi M, Jahanshahi M, Averbeck BB (2010) Effects of dopamine medication on sequence learning with stochastic feedback in Parkinson's disease. Front Syst Neurosci 4.
71. Shohamy D, Myers CE, Geghman KD, Sage J, Gluck MA, (2006) L-dopa impairs learning, but spares generalization, in Parkinson's disease. Neuropsychologia 44: 774-784.
72. Torta DM, Castelli L, Zibetti M, Lopiano L, Geminiani G, (2009) On the role of dopamine replacement therapy in decision-making, working memory, and reward in Parkinson's disease: does the therapy-dose matter? Brain Cogn 71: 84-91.
73. Macdonald PA, Monchi O, (2011) Differential effects of dopaminergic therapies on dorsal and ventral striatum in Parkinson's disease: implications for cognitive function. Parkinsons Dis 2011: 572743.
74. Gotham AM, Brown RG, Marsden CD, (1988) 'Frontal' cognitive function in patients with Parkinson's disease 'on' and 'off' levodopa. Brain 111 (Pt 2): 299-321.
75. Ghilardi MF, Feigin AS, Battaglia F, Silvestri G, Mattis P, et al. (2007) L-Dopa infusion does not improve explicit sequence learning in Parkinson's disease. Parkinsonism Relat Disord 13: 146-151.
76. Tremblay PL, Bedard MA, Langlois D, Blanchet PJ, Lemay M, et al. (2010) Movement chunking during sequence learning is a dopamine-dependant process: a study conducted in Parkinson's disease. Exp Brain Res 205: 375-385.
77. Cools R, Barker RA, Sahakian BJ, Robbins TW, (2001) Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. Cereb Cortex 11: 1136-1143.
78. Cools R, Ivry RB, D'Esposito M, (2006) The human striatum is necessary for responding to changes in stimulus relevance. J Cogn Neurosci 18: 1973-1983.
79. Cools R, Clark L, Owen AM, Robbins TW, (2002) Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J Neurosci 22: 4563-4567.
80. Dias R, Robbins TW, Roberts AC, (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380: 69-72.
81. Graef S, Biele G, Krugel LK, Marzinzik F, Wahl M, et al. (2010) Differential influence of levodopa on reward-based learning in Parkinson's disease. Front Hum Neurosci 4: 169.
82. Tomer R, Aharon-Peretz J, Tsitrinbaum Z, (2007) Dopamine asymmetry interacts with medication to affect cognition in Parkinson's disease. Neuropsychologia 45: 357-367.
83. Swainson R, Rogers RD, Sahakian BJ, Summers BA, Polkey CE, et al. (2000) Probabilistic learning and reversal deficits in patients with Parkinson's disease or frontal or temporal lobe lesions: possible adverse effects of dopaminergic medication. Neuropsychologia 38: 596-612.
84. Frank MJ, Seeberger LC, O'Reilly R C, (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306: 1940-1943.
85. Breitenstein C, Korsukewitz C, Floel A, Kretzschmar T, Diederich K, et al. (2006) Tonic dopaminergic stimulation impairs associative learning in healthy subjects. Neuropsychopharmacology 31: 2552-2564.
86. Pizzagalli DA, Evins AE, Schetter EC, Frank MJ, Pajtas PE, et al. (2008) Single dose of a dopamine agonist impairs reinforcement learning in humans: behavioral evidence from a laboratory-based measure of reward responsiveness. Psychopharmacology (Berl) 196: 221-232.
87. Santesso DL, Evins AE, Frank MJ, Schetter EC, Bogdan R, et al. (2009) Single dose of a dopamine agonist impairs reinforcement learning in humans: evidence from event-related potentials and computational modeling of striatal-cortical function. Hum Brain Mapp 30: 1963-1976.
88. Benke T, Delazer M, Bartha L, Auer A, (2003) Basal ganglia lesions and the theory of fronto-subcortical loops: neuropsychological findings in two patients with left caudate lesions. Neurocase 9: 70-85.
89. Rieger M, Gauggel S, Burmeister K, (2003) Inhibition of ongoing responses following frontal, nonfrontal, and basal ganglia lesions. Neuropsychology 17: 272-282.
90. Su CY, Chen HM, Kwan AL, Lin YH, Guo NW, (2007) Neuropsychological impairment after hemorrhagic stroke in basal ganglia. Arch Clin Neuropsychol 22: 465-474.
91. Reiss JP, Campbell DW, Leslie WD, Paulus MP, Stroman PW, et al. (2005) The role of the striatum in implicit learning: a functional magnetic resonance imaging study. Neuroreport 16: 1291-1295.
92. Helie S, Roeder JL, Ashby FG, (2010) Evidence for cortical automaticity in rule-based categorization. J Neurosci 30: 14225-14234.
93. Seger CA, Peterson EJ, Cincotta CM, Lopez-Paniagua D, Anderson CW, (2010) Dissociating the contributions of independent corticostriatal systems to visual categorization learning through the use of reinforcement learning modeling and Granger causality modeling. Neuroimage 50: 644-656.
94. Aarsland D, Litvan I, Salmon D, Galasko D, Wentzel-Larsen T, et al. (2003) Performance on the dementia rating scale in Parkinson's disease with dementia and dementia with Lewy bodies: comparison with progressive supranuclear palsy and Alzheimer's disease. J Neurol Neurosurg Psychiatry 74: 1215-1220.
95. Nelson HE, Willison J (1991) National adult reading test (NART). Windsor: NFER-Nelson. 1 portfolio.