Effects of aging and dopamine genotypes on the emergence of explicit memory during sequence learning

Neuropsychologia

Volumn 51, Issue 13, 2013, Pages 2757-2769

  Schuck, Nicolas W ^a,b   Frensch, Peter A ^b   Schjeide, Brit Maren M ^c   Schröder, Julia ^c,d   Bertram, Lars ^c   Li, Shu Chen ^a,e  

^a MAX PLANCK INSTITUTE FOR HUMAN DEVELOPMENT   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Aging; DARPP 32; DAT; Dopamine; Implicit and Explicit Memory; Sequence Learning; Serial Reaction Time Task

Indexed keywords

CYCLIC AMP; DOPAMINE; DOPAMINE RECEPTOR; PHOSPHOPROTEIN;

ADULT; AGED; AGING; ARTICLE; CAUCASIAN; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; EXPLICIT MEMORY; FEMALE; FRONTAL CORTEX; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HUMAN; IMPLICIT MEMORY; LEARNING; MAJOR CLINICAL STUDY; MALE; MEMORY; MOTOR PERFORMANCE; NEUROMODULATION; PHENOTYPE; REACTION TIME; TEMPORAL LOBE; VARIABLE NUMBER OF TANDEM REPEAT;

AGING; DARPP-32; DAT; DOPAMINE; IMPLICIT AND EXPLICIT MEMORY; SEQUENCE LEARNING; SERIAL REACTION TIME TASK;

ADULT; AGE FACTORS; AGED; AGING; DOPAMINE; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; FEMALE; GENOTYPE; HUMANS; MALE; MEMORY; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUESTIONNAIRES; REACTION TIME; SERIAL LEARNING; VERBAL LEARNING; YOUNG ADULT;

EID: 84886244079     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2013.09.009     Document Type: Article

References (116)

1. Aizenstein H.J., Butters M.A., Clark K.A., Figurski J.L., Andrew Stenger V., Nebes R.D., et al. Prefrontal and striatal activation in elderly subjects during concurrent implicit and explicit sequence learning. Neurobiology of Aging 2006, 27(5):741-751. 10.1016/j.neurobiolaging.2005.03.017.
2. 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. 10.1093/cercor/bhg119.
3. Arnsten A. Catecholamine modulation of prefrontal cortical cognitive function. Trends in Cognitive Sciences 1998, 2(11):436-447. 10.1016/S1364-6613(98)01240-6.
4. Atallah H.E., Lopez-Paniagua D., Rudy J.W., O'Reilly R.C. Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nature Neuroscience 2007, 10(1):126-131. 10.1038/nn1817.
5. Bäckman L., Nyberg L., Lindenberger U., Li S.-C., Farde L. The correlative triad among aging, dopamine, and cognition: Current status and future prospects. Neuroscience and Biobehavioral Reviews 2006, 30(6):791-807. 10.1016/j.neubiorev.2006.06.005.
6. Bateup H.S., Santini E., Shen W., Birnbaum S., Valjent E., Surmeier D.J., et al. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(33):14845-14850. 10.1073/pnas.1009874107.
7. Bennett I.J., Howard J.H., Howard D.V. Age-related differences in implicit learning of subtle third-order sequential structure. Journals of Gerontology. Series B, Psychological Sciences and Social Sciences 2007, 62(2):P98-P103.
8. Bennett I.J., Madden D.J., Vaidya C.J., Howard J.H., Howard D.V. White matter integrity correlates of implicit sequence learning in healthy aging. Neurobiology of Aging 2011, 32(12):2317.e1-2317.e12. 10.1016/j.neurobiolaging.2010.03.017.
9. Bertolino A., Blasi G., Latorre V., Rubino V., Rampino A., Sinibaldi L., et al. Additive effects of genetic variation in dopamine regulating genes on working memory cortical activity in human brain. Journal of Neuroscience 2006, 26(15):3918-3922. 10.1523/JNEUROSCI.4975-05.2006.
10. Bertolino A., Di Giorgio A., Blasi G., Sambataro F., Caforio G., Sinibaldi L., et al. Epistasis between dopamine regulating genes identifies a nonlinear response of the human hippocampus during memory tasks. Biological Psychiatry 2008, 64(3):226-234. 10.1016/j.biopsych.2008.02.001.
11. Bertolino A., Fazio L., Di Giorgio A., Blasi G., Romano R., Taurisano P., et al. Genetically determined interaction between the dopamine transporter and the D2 receptor on prefronto-striatal activity and volume in humans. Journal of Neuroscience 2009, 29(4):1224-1234. 10.1523/JNEUROSCI.4858-08.2009.
12. Bo J., Seidler R.D. Spatial and symbolic implicit sequence learning in young and older adults. Experimental Brain Research. Experimentelle Hirnforschung. Expérimentation cérébrale 2010, 201(4):837-851.
13. Boonstra A.M., Kooij J.J.S., Buitelaar J.K., Oosterlaan J., Sergeant J.A., Heister J.G.A.M.A., et al. An exploratory study of the relationship between four candidate genes and neurocognitive performance in adult ADHD. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 2008, 147(3):397-402. 10.1002/ajmg.b.30595.
14. Bornstein A.M., Daw N.D. Dissociating hippocampal and striatal contributions to sequential prediction learning. European Journal of Neuroscience 2012, 35(7):1011-1023. 10.1111/j.1460-9568.2011.07920.x.
15. Bortz, J. (1999). Statistik für Sozialwissenschaftler (German Edition). Berlin: Springer.
16. Brehmer Y., Westerberg H., Bellander M., Fürth D., Karlsson S., Bäckman L. Working memory plasticity modulated by dopamine transporter genotype. Neuroscience Letters 2009, 467(2):117-120. 10.1016/j.neulet.2009.10.018.
17. Brené S., Lindefors N., Ehrlich M., Taubes T., Horiuchi A., Kopp J., et al. Expression of mRNAs encoding ARPP-16/19, ARPP-21, and DARPP-32 in human brain tissue. Journal of Neuroscience 1994, 14(3):985-998.
18. Buchner A., Brandt M. Further evidence for systematic reliability differences between explicit and implicit memory tests. Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology 2003, 56(2):193-209. 10.1080/02724980244000260.
19. Cheon K.-A., Ryu Y.-H., Kim J.-W., Cho D.-Y. The homozygosity for 10-repeat allele at dopamine transporter gene and dopamine transporter density in Korean children with attention deficit hyperactivity disorder: Relating to treatment response to methylphenidate. European Neuropsychopharmacology 2005, 15(1):95-101. 10.1016/j.euroneuro.2004.06.004.
20. Cleeremans A. Principles for implicit learning. How implicit is implicit learning? 1997, 196-234. Oxford University Press, Oxford. D. Berry (Ed.).
21. Cohen N.J., Squire L.R. Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science 1980, 210(4466):207-210.
22. Colantuoni C., Hyde T.M., Mitkus S., Joseph A., Sartorius L., Aguirre C., et al. Age-related changes in the expression of schizophrenia susceptibility genes in the human prefrontal cortex. Brain Structure and Function 2008, 213(1-2):255-271. 10.1007/s00429-008-0181-5.
23. Dennis N.A., Cabeza R. Age-related dedifferentiation of learning systems: An fMRI study of implicit and explicit learning. Neurobiology of Aging 2011, 32(12):2318.e17-2318.e30. 10.1016/j.neurobiolaging.2010.04.004.
24. Destrebecqz A., Cleeremans A. Can sequence learning be implicit? New evidence with the process dissociation procedure. Psychonomic Bulletin and Review 2001, 8(2):343-350.
25. Destrebecqz A., Peigneux P., Laureys S., Degueldre C., Del Fiore G., Aerts J., et al. The neural correlates of implicit and explicit sequence learning: Interacting networks revealed by the process dissociation procedure. Learning and Memory 2005, 12(5):480-490. 10.1101/lm.95605.
26. Doyon J., Benali H. Reorganization and plasticity in the adult brain during learning of motor skills. Current Opinion in Neurobiology 2005, 15(2):161-167. 10.1016/j.conb.2005.03.004.
27. Eppinger B., Schuck N.W., Nystrom L.E., Cohen J.D. Reduced striatal responses to reward prediction errors in older compared with younger adults. Journal of Neuroscience 2013, 33(24):9905-9912. 10.1523/JNEUROSCI.2942-12.2013.
28. Erixon-Lindroth N., Farde L., Wahlin T.-B.R., Sovago J., Halldin C., Bäckman L. The role of the striatal dopamine transporter in cognitive aging. Psychiatry Research 2005, 138(1):1-12. 10.1016/j.pscychresns.2004.09.005.
29. Ferdinand N.K., Rünger D., Frensch P.a., Mecklinger A. Event-related potential correlates of declarative and non-declarative sequence knowledge. Neuropsychologia 2010, 48(9):2665-2674. 10.1016/j.neuropsychologia.2010.05.013.
30. Fleischman D.A., Wilson R.S., Gabrieli J.D.E., Bienias J.L., Bennett D.A. A longitudinal study of implicit and explicit memory in old persons. Psychology and Aging 2004, 19(4):617-625. 10.1037/0882-7974.19.4.617.
31. Frank M.J., Doll B.B., Oas-Terpstra J., Moreno F. Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. Nature Neuroscience 2009, 12(8):1062-1068. 10.1038/nn.2342.
32. 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. 10.1073/pnas.0706111104.
33. Frensch P.A., Rünger D. Implicit learning. Current Directions in Psychological Science 2003, 12:13-18.
34. Fuke S., Suo S., Takahashi N., Koike H., Sasagawa N., Ishiura S. The VNTR polymorphism of the human dopamine transporter (DAT1) gene affects gene expression. Pharmacogenomics Journal 2001, 1(2):152-156.
35. Gaillard V., Destrebecqz A., Michiels S., Cleeremans A. Effects of age and practice in sequence learning: A graded account of ageing, learning, and control. European Journal of Cognitive Psychology 2009, 21(2):255-282. 10.1080/09541440802257423.
36. Gheysen F., Van Opstal F., Roggeman C., Van Waelvelde H., Fias W. Hippocampal contribution to early and later stages of implicit motor sequence learning. Experimental Brain Research 2010, 202(4):795-807. 10.1007/s00221-010-2186-6.
37. Ghilardi M.F., Moisello C., Silvestri G., Ghez C., Krakauer J.W. Learning of a sequential motor skill comprises explicit and implicit components that consolidate differently. Journal of neurophysiology 2009, 101(5):2218-2229. 10.1152/jn.01138.2007.
38. Green A.E.A.E., Munafò M.R., DeYoung C.G.C.G., Fossella J.A.J.A., Fan J., Gray J.R. Using genetic data in cognitive neuroscience: From growing pains to genuine insights. Nature Reviews Neuroscience 2008, 9(9):710-720. 10.1038/nrn2461.
39. Haider H., Frensch P.A. The generation of conscious awareness in an incidental learning situation. Psychological Research 2005, 59(6):399-411.
40. Hämmerer D., Biele G., Müller V., Thiele H., Nürnberg P., Heekeren H.R., et al. Effects of PPP1R1B (DARPP-32) polymorphism on feedback-related brain potentials across the life span. Frontiers in Psychology 2013, 4:89. 10.3389/fpsyg.2013.00089.
41. Heinz A., Goldman D., Jones D.W., Palmour R., Hommer D., Gorey J.G., et al. Genotype influences in vivo dopamine transporter availability in human striatum. Neuropsychopharmacology 2000, 22(2):133-139. 10.1016/S0893-133X(99)00099-8.
42. Howard D.V., Howard J.H. Age differences in learning serial patterns: Direct versus indirect measures. Psychology and Aging 1989, 4(3):357-364.
43. Howard D.V., Howard J.H. Adult age differences in the rate of learning serial patterns: Evidence from direct and indirect tests. Psychology and Aging 1992, 7(2):232-241. 10.1037//0882-7974.7.2.232.
44. Howard D.V., Howard J.H., Japikse K., DiYanni C., Thompson A., Somberg R. Implicit sequence learning: Effects of level of structure, adult age, and extended practice. Psychology and Aging 2004, 19(1):79-92. 10.1037/0882-7974.19.1.79.
45. Howard J.H., Howard D.V. Age differences in implicit learning of higher order dependencies in serial patterns. Psychology and Aging 1997, 12(4):634-656.
46. Jacobsen L., Staley J. Prediction of dopamine transporter binding availability by genotype: A preliminary report. American Journal of Psychiatry 2000, 157(10):1700-1703.
47. Jacoby L.L. A process dissociation framework: Separating automatic from intentional uses of memory. Journal of Memory and Language 1991, 30(5):513-541. 10.1016/0749-596X(91)90025-F.
48. Kaasinen V., Vilkman H., Hietala J., Nagren K., Helenius H., Olsson H., et al. Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain. Neurobiology of Aging 2000, 21(5):683-688. 10.1016/S0197-4580(00)00149-4.
49. Karabanov A., Cervenka S., de Manzano O., Forssberg H., Farde L., Ullén F. Dopamine D2 receptor density in the limbic striatum is related to implicit but not explicit movement sequence learning. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(16):7574-7579. 10.1073/pnas.0911805107.
50. Kenward M.G., Roger J.H. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 1997, 53(3):983-997.
51. Li S.-C., Chicherio C., Nyberg L., von Oertzen T., Nagel I.E., Papenberg G., et al. Ebbinghaus revisited: Influences of the BDNF Val66Met polymorphism on backward serial recall are modulated by human aging. Journal of Cognitive Neuroscience 2010, 22(10):2164-2173. 10.1162/jocn.2009.21374.
52. Li S.-C., Lindenberger U., Bäckman L. Dopaminergic modulation of cognition across the life span. Neuroscience and Biobehavioral Reviews 2010, 34(5):625-630. 10.1016/j.neubiorev.2010.02.003.
53. Li S.-C., Lindenberger U., Frensch P.A. Unifying cognitive aging: From neuromodulation to representation to cognition. Neurocomputing 2000, 32-33(1-4):879-890. 10.1016/S0925-2312(00)00256-3.
54. Li S.-C., Lindenberger U., Hommel B., Aschersleben G., Prinz W., Baltes P.B. Transformations in the couplings among intellectual abilities and constituent cognitive processes across the life span. Psychological Science 2004, 15(3):155-163.
55. Li S.-C., Lindenberger U., Sikström S. Aging cognition: From neuromodulation to representation. Trends in Cognitive Sciences 2001, 5(11):479-486.
56. Li S.-C., Naveh-Benjamin M., Lindenberger U. Aging neuromodulation impairs associative binding: A neurocomputational account. Psychological Science 2005, 16(6):445-450. 10.1111/j.0956-7976.2005.01555.x.
57. Li S.-C., Papenberg G., Nagel I.E., Preuschhof C., Schröder J., Nietfeld W., et al. Aging magnifies the effects of dopamine transporter and D2 receptor genes on backward serial memory. Neurobiology of Aging 2013, 34(1):358.e1-358.e10. 10.1016/j.neurobiolaging.2012.08.001.
58. Li S.-C., Passow S., Nietfeld W., Schröder J., Bertram L., Heekeren H.R., et al. Dopamine modulates attentional control of auditory perception: DARPP-32 (PPP1R1B) genotype effects on behavior and cortical evoked potentials. Neuropsychologia 2013, 51(8):1649-1661. 10.1016/j.neuropsychologia.2013.04.005.
59. Li S.-C., Sikström S. Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation. Neuroscience and Biobehavioral Reviews 2002, 26(7):795-808.
60. Light L.L., Singh A. Implicit and explicit memory in young and older adults. Journal of Experimental Psychology: Learning, Memory, and Cognition 1987, 13(4):531-541.
61. Lim M.-H., Kim H.W., Paik K.-C., Cho S.C., Yoon D.Y., Lee H.-J. Association of the DAT1 polymorphism with attention deficit hyperactivity disorder (ADHD): A family-based approach. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 2006, 141B(3):309-311. 10.1002/ajmg.b.30282.
62. Lindenberger U., Nagel I.E., Chicherio C., Li S.-C., Heekeren H.R., Bäckman L. Age-related decline in brain resources modulates genetic effects on cognitive functioning. Frontiers in Neuroscience 2008, 2(2):234-244. 10.3389/neuro.01.039.2008.
63. Luce R.D. Response times: Their role in inferring elementary mental organization 1991, Oxford University Press, USA, (p. 584).
64. Meyer-Lindenberg A., Straub R.E., Lipska B.K., Verchinski B.A., Goldberg T., Callicott J.H., et al. Genetic evidence implicating DARPP-32 in human frontostriatal structure, function, and cognition. Journal of Clinical Investigation 2007, 117(3):672-682. 10.1172/JCI30413.
65. Miller G., Madras B. Polymorphisms in the 3'-untranslated region of human and monkey dopamine transporter genes affect reporter gene expression. Molecular Psychiatry 2002, 7(1):44-55. 10.1038/sj/mp/4000921.
66. Moisello C., Avanzino L., Tacchino A., Ruggeri P., Ghilardi M.F., Bove M. Motor sequence learning: Acquisition of explicit knowledge is concomitant to changes in motor strategy of finger opposition movements. Brain Research Bulletin 2011, 85(3-4):104-108. 10.1016/j.brainresbull.2011.03.023.
67. Moisello C., Crupi D., Tunik E., Quartarone A., Bove M., Tononi G., et al. The serial reaction time task revisited: A study on motor sequence learning with an arm-reaching task. Experimental Brain Research. Experimentelle Hirnforschung. Expérimentation cérébrale 2009, 194(1):143-155. 10.1007/s00221-008-1681-5.
68. 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. 10.1037/0735-7044.118.2.438.
69. Nagel I.E., Chicherio C., Li S.-C., von Oertzen T., Sander T., Villringer A., et al. Human aging magnifies genetic effects on executive functioning and working memory. Frontiers in Human Neuroscience 2008, 2:1. 10.3389/neuro.09.001.2008.
70. Nissen M.J., Bullemer P. Attentional requirements of learning: Evidence from performance measures. Cognitive Psychology 1987, 19(1):1-32. 10.1016/0010-0285(87)90002-8.
71. Papenberg G., Bäckman L., Chicherio C., Nagel I.E., Heekeren H.R., Lindenberger U., et al. Higher intraindividual variability is associated with more forgetting and dedifferentiated memory functions in old age. Neuropsychologia 2011, 49(7):1879-1888. 10.1016/j.neuropsychologia.2011.03.013.
72. Papenberg G., Bäckman L., Nagel I.E., Nietfeld W., Schröder J., Bertram L., et al. Dopaminergic gene polymorphisms affect long-term forgetting in old age: Further support for the magnification hypothesis. Journal of Cognitive Neuroscience 2013, 25(4):571-579. 10.1162/jocn_a_00359.
73. Pascual-Leone A., Grafman J., Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 1994, 263(5151):1287-1289.
74. Payton A. The impact of genetic research on our understanding of normal cognitive ageing: 1995 To 2009. Neuropsychology Review 2009, 19(4):451-477. 10.1007/s11065-009-9116-z.
75. Perruchet P., Bigand E., Benoit-Gonin F. The emergence of explicit knowledge during the early phase of learning in sequential reaction time tasks. Psychological Research 1997, 60(1-2):4-13. 10.1007/BF00419676.
76. R Development Core Team R: A language and environment for statistical computing 2011, R Foundation for Statistical Computing, Vienna, Austria.
77. 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. Human Brain Mapping 1997, 5(2):124-132.
78. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., et al. Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cerebral Cortex 2005, 15(11):1676-1689. 10.1093/cercor/bhi044.
79. Reber A.S. Implicit learning and tacit knowledge. Journal of Experimental Psychology: General 1989, 118(3):219-235. 10.1037/0096-3445.118.3.219.
80. Reber P.J., Squire L.R. Parallel brain systems for learning with and without awareness. Learning and Memory 1994, 1(4):217-229. 10.1101/lm.1.4.217.
81. Reed J., Johnson P. Assessing implicit learning with indirect tests: Determining what is learned about sequence structure. Journal of Experimental Psychology: Learning, Memory, and Cognition 1994, 20(3):585-594. 10.1037/0278-7393.20.3.585.
82. Rieckmann A., Bäckman L. Implicit learning in aging: Extant patterns and new directions. Neuropsychology Review 2009, 19(4):490-503. 10.1007/s11065-009-9117-y.
83. Rieckmann A., Fischer H., Bäckman L. Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: Relations to performance. NeuroImage 2010, 50(3):1303-1312. 10.1016/j.neuroimage.2010.01.015.
84. 11C]raclopride. Journal of Cerebral Blood Flow and Metabolism 1993, 13(2):310-314. 10.1038/jcbfm.1993.39.
85. Rodriguez S., Gaunt T.R., Day I.N.M. Hardy-Weinberg equilibrium testing of biological ascertainment for mendelian randomization studies. American Journal of Epidemiology 2009, 169(4):505-514. 10.1093/aje/kwn359.
86. Rommelse N.N.J., Altink M.E., Arias-Vásquez A., Buschgens C.J.M., Fliers E., Faraone S.V., et al. A review and analysis of the relationship between neuropsychological measures and DAT1 in ADHD. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 2008, 147B(8):1536-1546. 10.1002/ajmg.b.30848.
87. Rose M., Haider H., Büchel C. The emergence of explicit memory during learning. Cerebral Cortex 2010, 20(12):2787-2797. 10.1093/cercor/bhq025.
88. Rünger D., Frensch P.A. How incidental sequence learning creates reportable knowledge: The role of unexpected events. Journal of Experimental Psychology: Learning, Memory, and Cognition 2008, 34(5):1011-1026. 10.1037/a0012942.
89. Rünger D., Frensch P.A. Defining consciousness in the context of incidental sequence learning: Theoretical considerations and empirical implications. Psychological Research 2010, 74(2):121-137. 10.1007/s00426-008-0225-8.
90. Santini E., Valjent E., Usiello A., Carta M., Borgkvist A., Girault J.-A., et al. Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in l-DOPA-induced dyskinesia. Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2007, 27(26):6995-7005. 10.1523/JNEUROSCI.0852-07.2007.
91. Schott B.H., Seidenbecher C.I., Fenker D.B., Lauer C.J., Bunzeck N., Bernstein H.-G., et al. The dopaminergic midbrain participates in human episodic memory formation: Evidence from genetic imaging. Journal of Neuroscience 2006, 26(5):1407-1417. 10.1523/JNEUROSCI.3463-05.2006.
92. Schuck N.W., Doeller C.F., Schjeide B.-M.M., Schröder J., Frensch P.A., Bertram L., et al. Aging and KIBRA/WWC1 genotype affect spatial memory processes in a virtual navigation task. Hippocampus 2013, 23(10):919-930. 10.1002/hipo.22148.
93. Schuck N.W., Gaschler R., Frensch P.A. Implicit learning of what comes when and where within a sequence: The time-course of acquiring serial position-item and item-item associations to represent serial order. Advances in Cognitive Psychology 2012, 8(2):83-97. 10.2478/v10053-008-0106-0.
94. Schuck N.W., Gaschler R., Keisler A., Frensch P.a. Position-item associations play a role in the acquisition of order knowledge in an implicit serial reaction time task. Journal of Experimental Psychology. Learning, Memory, and Cognition 2012, 38(2):440-456. 10.1037/a0025816.
95. Scimeca J.M., Badre D. Striatal contributions to declarative memory retrieval. Neuron 2012, 75(3):380-392. 10.1016/j.neuron.2012.07.014.
96. Seamans J.K., Yang C.R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Progress in Neurobiology 2004, 74(1):1-58. 10.1016/j.pneurobio.2004.05.006.
97. Seidler R.D., Tuite P., Ashe J. Selective impairments in implicit learning in Parkinson's disease. Brain Research 2007, 1137(1):104-110. 10.1016/j.brainres.2006.12.057.
98. Shanks D.R., St.John M.F. Characteristics of dissociable human learning systems. Behavioral and Brain Sciences 1994, 17(03):367-395. 10.1017/S0140525X00035032.
99. Simon J.R., Stollstorff M., Westbay L.C., Vaidya C.J., Howard J.H., Howard D.V. Dopamine transporter genotype predicts implicit sequence learning. Behavioural Brain Research 2011, 216(1):452-457. 10.1016/j.bbr.2010.08.043.
100. Simon J.R., Vaidya C.J., Howard J.H., Howard D.V. The effects of aging on the neural basis of implicit associative learning in a probabilistic triplets learning task. Journal of Cognitive Neuroscience 2012, 24(2):451-463. 10.1162/jocn_a_00116.
101. Song S., Marks B., Howard J.H., Howard D.V. Evidence for parallel explicit and implicit sequence learning systems in older adults. Behavioural Brain Research 2009, 196(2):328-332. 10.1016/j.bbr.2008.09.022.
102. Squire L.R. Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory 2004, 82(3):171-177. 10.1016/j.nlm.2004.06.005.
103. Squire L.R. Memory and brain systems: 1969-2009. Journal of Neuroscience 2009, 29(41):12711-12716. 10.1523/JNEUROSCI.3575-09.2009.
104. Squire L.R., Zola-Morgan S. The medial temporal lobe memory system. Science 1991, 253(5026):1380.
105. Svenningsson P., Nishi A., Fisone G., Girault J.-A., Nairn A.C., Greengard P. DARPP-32: An integrator of neurotransmission. Annual Review of Pharmacology and Toxicology 2004, 44:269-296. 10.1146/annurev.pharmtox.44.101802.121415.
106. van de Giessen E.M., de Win M.M.L., Tanck M.W.T., van den Brink W., Baas F., Booij J. Striatal dopamine transporter availability associated with polymorphisms in the dopamine transporter gene SLC6A3. Journal of Nuclear Medicine 2009, 50(1):45-52. 10.2967/jnumed.108.053652.
107. Van Dyck C.H., Seibyl J.P., Malison R.T., Laruelle M., Zoghbi S.S., Baldwin R.M., et al. Age-related decline in dopamine transporters: Analysis of striatal subregions, nonlinear effects, and hemispheric asymmetries. American Journal of Geriatric Psychiatry 2002, 10(1):36-43.
108. Vandenbergh D., Persico A., Hawkins A. Human dopamine transporter gene (DAT1) maps to chromosome 5p15. 3 and displays a VNTR. Genomics 1992, 14(4):1104-1106.
109. VanNess S.H., Owens M.J., Kilts C.D. The variable number of tandem repeats element in DAT1 regulates in vitro dopamine transporter density. BMC Genetics 2005, 6:55. 10.1186/1471-2156-6-55.
110. Verwey W.B. Diminished motor skill development in elderly: Indications for limited motor chunk use. Acta Psychologica 2010, 134(2):206-214. 10.1016/j.actpsy.2010.02.001.
111. Verwey W.B., Abrahamse E.L., Ruitenberg M.F.L., Jiménez L., de Kleine E. Motor skill learning in the middle-aged: Limited development of motor chunks and explicit sequence knowledge. Psychological Research 2011, 75(5):406-422. 10.1007/s00426-011-0320-0.
112. Vijayraghavan S., Wang M., Birnbaum S.G., Williams G.V., Arnsten A.F.T. Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nature Neuroscience 2007, 10(3):376-384. 10.1038/nn1846.
113. Walhovd K.B., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., et al. Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiology of Aging 2011, 32(5):916-932. 10.1016/j.neurobiolaging.2009.05.013.
114. Wessel J.R., Haider H., Rose M. The transition from implicit to explicit representations in incidental learning situations: More evidence from high-frequency EEG coupling. Experimental Brain Research. Experimentelle Hirnforschung. Expérimentation cérébrale 2012, 217(1):153-162. 10.1007/s00221-011-2982-7.
115. Willingham D.B., Goedert-Eschmann K. The relation between implicit and explicit learning: Evidence for parallel development. Psychological Science 1999, 10(6):531-534. 10.1111/1467-9280.00201.
116. Yger M., Girault J.-A. DARPP-32, Jack of all trades... Master of which?. Frontiers in Behavioral Neuroscience 2011, 5(September):56. 10.3389/fnbeh.2011.00056.